subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex...

Subdivisions of Auditory Cortexand Ipsilateral Cortical Connections

of the Parabelt Auditory Cortexin Macaque Monkeys

T.A. HACKETT, I. STEPNIEWSKA, AND J.H. KAAS*Department of Psychology, Vanderbilt University, Nashville, Tennessee 37240

ABSTRACTAuditory cortex of macaque monkeys can be divided into a core of primary or primary-like

areas located on the lower bank of the lateral sulcus, a surrounding narrow belt of associatedfields, and a parabelt region just lateral to the belt on the superior temporal gyrus. Wedetermined patterns of ipsilateral cortical connections of the parabelt region by placinginjections of four to seven distinguishable tracers in each of five monkeys. Results were relatedto architectonic subdivisions of auditory cortex in brain sections cut parallel to the surface ofartificially flattened cortex (four cases) or cut in the coronal plane (one case). An auditory corewas clearly apparent in these sections as a 16- to 20-mm rostrocaudally elongated oval,several millimeters from the lip of the sulcus, that stained darkly for parvalbumin, myelin,and acetylcholinesterase. These features were most pronounced caudally in the cortexassigned to auditory area I, only slightly reduced in the rostral area, and most reduced in thenarrower rostral extension we define as the rostrotemporal area. A narrow band of cortexsurrounding the core stained more moderately for parvalbumin, acetylcholinesterase, andmyelin. Two regions of the caudal belt, the caudomedial area, and the mediolateral area,stained more darkly, especially for parvalbumin. Rostromedial and medial rostrotemporal,regions of the medial belt stained more lightly for parvalbumin than the caudomedial area orthe lateral belt. The parabelt region stained less darkly than the core and belt fields. Injectionsconfined to the parabelt region labeled few neurons in the core, but large numbers in parts ofthe belt, the parabelt, and adjacent portions of the temporal lobe. Injections that encroachedon the belt labeled large numbers of neurons in the core and helped define the width of thebelt. Caudal injections in the parabelt labeled caudal portions of the belt, rostral injectionslabeled rostral portions, and both caudal and rostral injections labeled neurons in therostromedial area of the medial belt. These observations support the concept of dividing theauditory cortex into core, belt, and parabelt; provide evidence for including the rostral area inthe core; suggest the existence of as many as seven or eight belt fields; provide evidence for atleast two subdivisions of the parabelt; and identify regions of the temporal lobe involved inauditory processing. J. Comp. Neurol. 394:475–495, 1998. r 1998 Wiley-Liss, Inc.

Indexing terms: association cortex; temporal lobe; primate; architectonics

In the present report, we evaluate and extend anemerging theory of auditory cortex organization in ma-caque monkeys and other primates. The general location ofauditory cortex has long been known from the observa-tions that lesions of cortex of the lower bank of the lateralfissure produce degeneration within the medial geniculatecomplex of the thalamus (Walker, 1937; Mesulam andPandya, 1973) and that auditory stimuli evoke neuralactivity in this cortex (Licklider and Kryter, 1942; Adesand Felder, 1942; Walzl and Woolsey, 1943). Pandya andSanides (1973) subsequently made an important distinc-

tion between a koniocortical or granular primary-like‘‘core’’ of auditory cortex projecting to a surrounding ‘‘belt’’of several architectonic fields. At this time, Merzenich and

Grant sponsor: NINDS; Grant number: NS 16446; Grant sponsor:NIDCD; Grant number: DC 00249.

*Correspondence to: Jon H. Kaas, Ph.D., Vanderbilt University, Depart-ment of Psychology, 301 Wilson Hall, 111 21st Avenue South, Nashville, TN37240. E-mail: [email protected]

Received 22 September 1997; Revised 31 December 1997; Accepted 8January 1998

THE JOURNAL OF COMPARATIVE NEUROLOGY 394:475–495 (1998)

r 1998 WILEY-LISS, INC.

Brugge (1973) described tonotopic maps in relation toarchitectonic fields and divided the primary-like region, orcore, into at least two fields: the primary area, auditoryarea I (AI); and an adjoining rostral field, first named RLfor rostrolateral and later simply as R for rostral (Imig etal., 1977). Merzenich and Brugge (1973) also divided thesurrounding belt cortex into several fields, including caudo-medial (CM) and lateral (L) fields with evidence of tono-topic organization. Morel and Kaas (1992) concluded thatthe auditory core includes a third primary-like field, RT forrostrotemporal, with a third sequence of tonotopic organi-zation and somewhat muted koniocortical features. Eachof these core fields is further characterized by direct inputsfrom the ventral division of the medial geniculate complex.Cortical connection patterns in these monkeys providedevidence for as many as seven belt areas (also see Fitzpa-trick and Imig, 1980), and projections from lateral beltareas helped define an auditory parabelt region within theadjoining superior temporal cortex. Similar anatomicalobservations were subsequently made on macaque mon-keys (Morel et al., 1993; Jones et al., 1995), suggesting thatauditory cortex is subdivided as in owl monkeys. Inaddition, microelectrode recordings have been used toreveal three tonotopic patterns in the cortex of the lateralbelt of macaque monkeys (Rauschecker et al., 1995). Insummary, auditory processing in monkeys seems to in-clude a core of three primary-like areas with direct medialgeniculate complex inputs (Morel et al., 1993; Molinari etal., 1995), a relay from core areas to a surrounding belt ofapproximately seven or eight fields, and a relay from thelateral belt to a lateral parabelt with possible subdivisions.

In the present study, we investigated parts of thisgeneral proposal by injecting several distinguishable trac-ers at different locations along the length of the lateralparabelt region. The locations of injections that labeledneurons in the core or belt regions further defined theextent of the lateral parabelt. In addition, topographicpatterns of connections with the parabelt provided evi-dence for subdivisions of areas of the belt and core.Likewise, connections of different parts of the parabeltprovided evidence for subdivisions of the parabelt. Finally,connections of the parabelt identified additional regions ofthe cortex that are likely to be involved in auditory

processing. Some of the results have been briefly presentedelsewhere (Hackett et al., 1995).

MATERIALS AND METHODS

Surgical procedures

All surgical procedures were performed under asepticconditions in a surgical suite in strict adherence to theVanderbilt University Animal Care Committee guidelinesand the Animal Welfare Act. Five adult macaque monkeys(three Macaca mulatta, two Macaca nemestrina) werepremedicated with dexamethasone (1 mg/kg, IM), atropinesulfate (0.5 mg/kg), and penicillin G (10,000 units, IM).Anesthesia was induced by ketamine hydrochloride (10mg/kg, IM); thereafter, the animals were intubated andmaintained on 1–2% isoflurane during all surgical proce-dures. An intravenous catheter was inserted for adminis-tration of lactated Ringer’s solution. Body temperaturewas maintained at 38oC with a water-circulating heatingpad. Vital signs and CO2 levels were continuously moni-tored and used to adjust the level of anesthesia.

The head of the monkey was stabilized in a stereotaxicinstrument (David Kopf Instruments, Tujunga, CA). Amidline incision was made exposing the skull, followed byretraction of the left temporal muscle. A craniotomy wasperformed, exposing the superior temporal gyrus and theoverlying parietofrontal cortex. The dura was cut andretracted. Warm saline was applied to the brain periodi-cally to prevent dessication of the cortex during photogra-phy and tracer injections. Photographs of the corticalsurface were then taken for subsequent reconstruction ofinjection sites in relation to the sulci and blood vessels.After injections of all tracers, the dural flap was sutured,and the exposed area of the brain was covered withsoftened gelfilm. The opening in the skull was closed withdental acrylic. The temporal muscle and skin were suturedinto place over the skull. Antibiotic gel was applied alongthe suture line.

After surgery, the endotracheal tube was removed andvital signs were monitored during recovery from anesthe-sia. Once vital signs were stable, the animals were re-turned to their cages and monitored carefully until recov-

Abbreviations

AI auditory area I (primary auditory)AL anterior lateral auditory beltAS arcuate sulcusBDA biotinylated dextroamineC caudal auditory beltCiS circular sulcusCL caudal lateral auditory beltCM caudomedial auditory beltCP caudal auditory parabeltCS central sulcusDY diamidino yellowFB fast blueFR fluororubyGB rhodamine green beadsH high-frequency stimulusHRP horseradish peroxidaseILS inferior limiting sulcusIns insulaIPS intraparietal sulcusL low-frequency stimulusLRT lateral rostrotemporal auditory beltLS lateral sulcusLuS lunate sulcus

ML middle lateral auditory beltMRT medial rostrotemporal auditory beltMST medial superior temporal areaMT medial temporal areapaAc caudal parakoniocortical areapaAlt lateral parakoniocortical areaPi parainsular areaproA prokoniocortical areaPS principal sulcusR rostral area (primary auditory)RB rhodamine red beadsreIt retroinsular temporal areaRL rostrolateral areaRM rostromedial regionRP rostral auditory parabeltRT rostrotemporalRTL lateral rostrotemporal auditory beltRTM medial rostrotemporal auditory beltSTG superior temporal gyrusSTS superior temporal sulcusTP temporal poleTpt temporoparietal areaWB wide band stimulus

476 T.A. HACKETT ET AL.

ery was complete. Daily injections of penicillin G (10,000units, IM) were given for 5 to 7 days after surgery toprevent postoperative infection. Butorphanol (0.4 mg/kg)or Banamine (1 mg/kg) were administered as neededduring the first few days of the survival period for anal-gesia.

Tracer injections

In each case, microinjections of four to seven differentanatomical tracers were made at equal intervals along thedorsal superior temporal gyrus within 3 mm of the lateralsulcus in the left hemisphere. Injections were made with aglass micropipette sealed to the needle of a 1- or 5-µlHamilton syringe. The tracers used were horseradishperoxidase conjugated to wheat germ agglutinin (WGA-HRP); biotinylated dextroamine (BDA), and the followingfluorescent tracers: fast blue (FB); diamidino yellow (DY);fluororuby (FR); fluorescein (FS); rhodamine green beads(GB); and rhodamine red beads (RB). Because the tracersvary in sensitivity, the amounts and solution concentra-tions were varied accordingly (typically, 0.01 to 0.05 µl at2% for WGA-HRP; 0.1 to 0.3 µl at 2 to 10% for BDA andfluorescent tracers). The survival period was 7 days whenWGA-HRP was used (three cases) and 12 days when onlyfluorescent tracers or BDA were injected (two cases, 96-1,97-33).

Histologic procedures

At the end of the survival period, a lethal dose ofpentobarbital was administered. Just before cardiac ar-rest, the animals were perfused through the heart withwarm saline followed by cold 2% paraformaldehyde dis-solved in 0.1 M phosphate buffer. Immediately after perfu-sion, the brains were removed and photographed. In fourcases (94-64, 95-10, 96-1, 97-33), the cortex was separatedfrom the brainstem and cut mid-sagittally through thecorpus callosum. Each hemisphere was cut into blocksseparating the frontal and temporal lobes. The pia mattercovering the sulci was removed with forceps, and the whitematter was dissected away with a blunt probe. The sulciwere then unfolded, and the cortex was flattened betweenglass plates. The flattened blocks were soaked in 30%sucrose solution overnight, then cut parallel to the cortexat 40 µm on a freezing microtome. The thalamus was cuttraditionally in the frontal plane. In one case (95-52), theleft hemisphere and brainstem were soaked in 30% su-crose overnight, then cut at 50 mm in the coronal plane toreveal the laminar distribution of label in the cortex.Surface views of these sections were obtained by graphi-cally unfolding the cortex (see Morel and Bullier, 1990).

Alternate series of sections were processed for (1) fluores-cent microscopy; (2) WGA-HRP, by using a low-artifacttetramethyl benzidine (TMB) procedure (Gibson et al.,1984); (3) cytochrome oxidase (Wong-Riley, 1979); (4) ace-tylcholinesterase (Geneser-Jensen and Blackstad, 1971);(5) parvalbumin immunohistochemistry; (6) calbindin im-munohistochemistry; (7) Nissl staining with cresyl violet(coronal sections only); (8) myelinated fiber staining (Gall-yas, 1979); or (9) BDA (Sakai et al., 1996).

Data analysis

Cells labeled with fluorescent tracers were plotted underultraviolet illumination with a Leitz microscope coupled toan X-Y plotter (Bioquant System, R & M Biometrics, Inc.,

Nashville, TN). Cells labeled with WGA-HRP were plottedunder darkfield illumination with a drawing tube. Photo-graphs and drawings of each section were made, notinginjection sites, architectonic boundaries, the location ofblood vessels, and the distribution of labeled cells. Acomposite drawing was made from adjacent sections pro-cessed for label, cytochrome oxidase, acetylcholinesterase,parvalbumin, calbindin, Nissl, and myelin by aligningcommon architectonic features and blood vessels. Three-dimensional and surface-view composite images were com-posed for reconstruction of the cortex by using Canvas v.3.5 software (Deneba Software, Miami, FL), installed on aPower Macintosh 7200/75 computer (Apple Computers,Cupertino, CA). The final drawings were analyzed toreveal (1) the individual connection patterns of each tracerinjection, (2) the connection patterns of injections atsimilar or dissimilar locations, (3) consistency across cases,(4) aberrant or unusual patterns.

Darkfield photographs were made by using a 35-mmcamera mounted on a Wild M400 photomacroscope. Slidesof these sections were scanned in color at 253 dots per inchwith a Polaroid Sprint Scan color scanner and convertedinto gray scale by using Adobe Photoshop v. 4.0 software(Mountain View, CA). Brightfield images were acquireddirectly by using a Leaf Lumina digital scanning cameramounted on a Nikon E800 microscope. The digitizedimages were adjusted for brightness and contrast, cropped,and pasted into the final figure, onto which text was added.Except for contrast adjustment and cropping, the imageswere not altered in any way.

RESULTS

For descriptive purposes, we have divided the auditorycortex of the temporal lobe of macaque monkeys into threemain regions (Fig. 1). The auditory territory includes thecortex of the caudal superior temporal plane and theadjoining superior temporal sulcus (Fig. 1A). In the follow-ing pages, we present architectonic and connectional evi-dence that auditory cortex can be divided into a core regionsurrounded by a narrow belt, which is bordered laterallyby a parabelt. These subdivisions are shown on a partlyunfolded schematic of auditory cortex (Fig. 1B) as an aid tointerpretation of illustrations of cortical architecture andcortical connections shown in the following illustrations.

Cortical architecture and subdivisions

Architectonic features of the auditory cortex. Flat-tened sections processed for parvalbumin, myelinatedfibers (myelin), acetylcholinesterase (AChE), and cyto-chrome oxidase (CO) were examined for differences instaining density to reveal subdivisions of the auditorycortex. In flattened sections of the superior temporal lobe,an elongated region (16 to 20 mm), located medially on thesuperior temporal plane, stained darkly for parvalbumin,myelin, and acetylcholinesterase (Fig. 2). The cytochromeoxidase pattern (not shown) was patchy and not as usefulin the delineation of architectural boundaries in flattenedsections. The width of the darkly stained region decreasedfrom about 10-mm caudally to less than 2-mm rostrallyand was most intense from 400 to 800 µm below the pialsurface. Much of this region clearly corresponds to thecore, or primary auditory cortex, of other investigators.The caudal portion of the core (AI) was larger and stainedsomewhat more densely than the adjacent rostral area (R)

CONNECTIONS OF THE PARABELT AUDITORY CORTEX 477

in most sections. A smaller third subdivision located justrostral to R, corresponding in position to RT in owlmonkeys (Morel and Kaas, 1992), stained darkly forparvalbumin and myelin, and moderately for acetylcholin-esterase, but more weakly overall than AI and R. In someflattened sections AI and R could be distinguished as twodarkly stained elongated ovoids separated by a narrowband (1 to 2 mm) of somewhat lighter staining (see Fig. 2).In the three cases involving M. mulatta (94-64, 95-10,97-33), the darkly stained core region was longer and moreelongated than in the two M. nemestrina cases (95-52,96-1). AI, R, as well as RT, were more distinct in M.mulatta. In coronal sections the core region was character-ized by intense staining in lower layer III and layer IV(Fig. 3). In all cases the sizes and extents of the left andright core regions were comparable.

Low-magnification images of coronal sections immuno-stained for parvalbumin are shown in Figure 3 through AI,R, and RT. Neuropil staining in lower layer III and layer IVwas very dense in the subdivisions of the core (AI, R, RT).

Staining intensity was comparable in AI and R, andgenerally weaker in RT. The border between the core andsurrounding belt areas was characterized by diminishedstaining intensity in lower layer III and layer IV, as well asa reduction in the width of these layers. The transitionbetween the core and belt regions was particularly distinctat the level of RT, and less pronounced caudally in R andAI. Background neuropil staining for parvalbumin in layerI of the core was very light, interrupted by vertical bands ofmoderately immunostained fibers that spread out horizon-tally across upper layer I. The neuropil of layers II andupper III was moderately stained. Many cells in layer IIwere strongly reactive for parvalbumin. Neuropil staining inlayers V and VI was also moderate, and numerous parvalbu-min-positive cells were scattered throughout both layers.

Architectonic features of the auditory belt cortex. Anarrow band of cortex (2- to 4-mm wide) surrounding thedarkly stained core region stained moderately for parvalbu-min, acetylcholinesterase, and myelin. Staining in thisband was muted compared with the core, but less so in thelateral parabelt. The band is most apparent in panels B,D,and F of Figure 2. Adjacent to the caudal border of the coretwo smaller patches (CM, CL) stained darkly for parvalbu-min, acetylcholinesterase, and myelin. These areas occu-pied the approximate locations of the caudal belt areas,CM and C, identified by Morel and Kaas (1992) and Morelet al. (1993), and are labeled accordingly in Figure 2.Extending laterally from AI and CL to the edge of thelateral sulcus, the belt cortex of the caudal superiortemporal plane, labeled as ML in Figure 2, stained moder-ately for parvalbumin, acetylcholinesterase, and myelin.Rostrally, in AL, staining in the lateral belt region was lessintense. Our areas AL and ML correspond to areas AL andPL of Morel et al. (1993). PL was renamed to coincide withrecent physiologic studies of the superior temporal region(Rauschecker et al., 1995). In the cortex of circular sulcus(CiS), corresponding to the rostral medial belt areas RMand MRT (Morel et al., 1993), staining for acetylcholines-terase was moderate (see panels E and F). In contrast,myelination and immunoreactivity for parvalbumin ap-peared to be very weak in this region. No attempt wasmade to subdivide the belt region further in flattenedsections. In coronal sections the transition between thecore and the belt was gradual, making it difficult toestablish a precise border between the regions.

Immunoreactivity for parvalbumin in the belt was muchdifferent than in the core (Fig. 3). In the medial belt (RM,CM), the parvalbumin-reactive fibers that stretched verti-cally through layer I in the core were absent. Backgroundstaining of the neuropil in layers II and III was moderateand populated by numerous parvalbumin-positive cells.The neuropil in layer IV stained more darkly than in thesurrounding layers, but immunoreactivity was much lessintense than in the core. The neuropil of layers V and VIwas weakly immunoreactive for parvalbumin, and theircombined width was reduced. A small number of parvalbu-min-positive cells was scattered throughout layers V andVI. In the lateral belt (AL, ML) neuropil staining forparvalbumin was darker overall than in the medial belt,and more evenly distributed. Compared with the medialbelt the upper and lower boundaries of layer IV were lessdistinct, owing to darker immunoreactivity in layers IIIand V. The transition between the lateral belt and the core

Fig. 1. Proposed subdivisions of auditory cortex in macaque mon-keys. A: A lateral view of the brain showing major fissures (AS, arcuatesulcus; CS, central sulcus; IPS, intraparietal sulcus; LuS, lunatesulcus, LS, lateral sulcus; PS, principal sulcus; STS, superior temporalsulcus) and the auditory region of the superior temporal gyrus(shaded). B: A graphically unfolded view of the cortex of the lower bankof the lateral sulcus and the adjoining a superior temporal gyrus. Thelocations of the auditory core, belt, and parabelt are indicated. Forabbreviations, see list.


was more gradual than the transition between the medialbelt and the core. Overall, immunoreactivity in the beltregion was greater caudally.

Architectonic features of the auditory parabelt cor-

tex. A wide region adjacent to the lateral belt extendedbeyond the edge of the lateral sulcus onto the dorsalsurface of superior temporal gyrus. This area corresponds

to the auditory parabelt. The anatomical tracers used inthis study were injected along the rostrocaudal axis of thisregion near the ventral edge of the lateral sulcus. Thearrows in Figure 2 identify the location of the diamidinoyellow injection. In flattened sections, staining for parval-bumin, myelin, and acetylcholinesterase in the parabeltregion was patchy and generally lighter than in the belt

Parvalbumin

Myelin

Acetylcholinesterase

A B

C D

E F

RMRTM

RTL

ALML

CL

CMAIR

RTAI

AI

AI AI

Insula

LS

CPRP

AI

Fig. 2. A–F: The histochemistry of auditory cortex. Brain sectionswere cut parallel to the surface of artificially flattened cortex from case95-10 (see Fig. 5) and processed for parvalbumin, myelin, or acetylcho-linesterase. Sections in the left column are more superficial than thoseon the right. In all preparations, a large, dark oval corresponding tothe core auditory area I (AI) is apparent (the section in panel F is toodeep to reveal the darkness of AI in the center, but the ring around theoval reflects more superficial tissue). In most sections, the rostral core

area (R) is also apparent as a dark oval, whereas the rostrotemporalarea (RT) is most visible in B. Note also in B, slight differences in thedarkness of the caudomedial (CM), caudolateral (CL), middle lateral(ML), and anterolateral (AL), areas of the auditory belt. Dots outlinethese areas, as well as the lip of the lateral sulcus (LS). In all panels,an arrowhead marks the diamidino yellow injection site. For abbrevia-tions, see list. Scale bar 5 5 mm (applies to A–F).


areas, but no consistent rostrocaudal trends were ap-parent.

In coronal sections immunostained for parvalbumin(Fig. 3), the parabelt (RP, CP) exhibited architectural

properties that distinguished it from the core and beltregions. In layer IV, immunoreactivity for parvalbuminwas darker than in the surrounding layers, but muchlighter than in the core and lateral belt. Caudally, at thelevel of AI and R (Fig. 3B,C), the transition between thelateral belt and parabelt was distinct, as evidenced by anabrupt reduction in layer III/IV staining intensity at thelateral edge of the superior temporal plane. Rostrally, atthe level of RT (Fig. 3A), immunoreactivity for parvalbu-min was more uniform across the planum and gyralportions of the superior temporal gyrus. In the parabeltparvalbumin-positive fibers extended vertically throughlayer I, as in the core, but the number of fibers appeared tobe fewer. Background neuropil staining in layers II and IIIwas lighter than in the core and lateral belt, but slightlydarker and more uniform than in the medial belt. Theneuropil of layers V and VI stained moderately for parval-bumin and contained scattered large parvalbumin-posi-tive cells. Immunoreactivity was more intense in thecaudal parabelt.

Ipsilateral cortical connections of theauditory parabelt cortex

Injections in the parabelt labeled neurons in the medialbelt, lateral belt, parabelt, and superior temporal sulcus.Perhaps the most surprising result of this study was therelative absence of labeling throughout the core region(Figs. 4–7). Very few labeled cells were found in the coreafter injections restricted to the parabelt region on thesuperior temporal gyrus. When labeled cells were found inthe core after these injections the rostral two-thirds of theregion, corresponding to R and RT, generally containedmore labeled cells than the caudal third, corresponding toAI, which was almost always devoid of labeled cells.However, in case 95-52L (Fig. 8), there were a number oflabeled neurons in the core, including AI. These labeledcells were primarily associated with the three most caudalinjections: fast blue (open triangles), WGA-HRP (filledsquares), and diamidino yellow (open squares). Compari-son of the injection sites with adjacent Nissl sectionsrevealed that these three injections encroached upon thecortex of the lateral belt (Fig. 9), known to be directlyconnected with the core. Thus, the caudal three injectionsin case 95-52L (Fig. 8) help define the width of the belt byencroaching on the belt and thereby labeling neurons inthe core. In case 95-52L most of the label in the core wasconfined to AI, with bands of labeled neurons for eachinjection located at approximately the same rostrocaudallevel as the injection site. This pattern of connections isconsistent with the observation that adjacent areas of thebelt and core are more strongly interconnected than nonad-jacent areas (Morel and Kaas, 1992; Morel et al., 1993). Asimilar pattern was found in case 97-33L (Fig. 7).

In contrast to the nearly complete lack of cell labelingwithin the core, dense populations of labeled cells werefound in the surrounding belt, parabelt, and upper bank ofthe superior temporal sulcus. The distribution of retro-gradely labeled cells in the auditory belt and adjacentareas was topographic; that is, rostral injections tended tolabel rostral sites and caudal injections tended to labelcaudal sites, with variable degrees of overlap. The distribu-tions of labeled cells associated with the more sensitivetracers (e.g., fast blue, diamidino yellow, WGA-HRP) andclosely spaced injections tended to overlap more thanless-sensitive tracers (e.g., rhodamine red and green beads)

RT

AL

R

RM

RP

CM

AI MLCP

C

B

A

Fig. 3. The distribution of parvalbumin in coronal sections throughthe auditory cortex of M. mulatta (case 97-33, see Fig. 7). A: The mostrostral section shows that core area rostrotemporal area (RT) stainedmoderately dark. B: More caudally, the core area R stained quite dark,whereas the rostromedial (RM) and anterolateral (AL) belt areas areless dark. C: Most caudally, core auditory area I (AI) stained veryintensely, middle lateral belt area (ML), was moderately dark, and thecaudomedial belt area (CM) was somewhat less dark. Note also thatthe caudal parabelt (CP) in C is slightly darker than the rostralparabelt (RP) in B. Arrowheads indicate boundaries between areas.Scale bar 5 2 mm (applies to A–C).


and widely spaced injections. In general, injections placedin the parabelt caudal to the AI/R border primarily labeledcells in the lateral belt, parabelt, and STS at sites caudal tothis border. Likewise, injections placed rostral to the AI/Rborder tended to label cells in the rostral auditory cortex.This trend was most obvious in cases 95-10L (Fig. 5) and96-1L (Fig. 6). In case 95-10L, the fast blue (filled circles)and green beads (filled squares) injections were placedrostral to the putative border of AI and R. The distributionof labeled cells associated with these injections was largelyrestricted to the lateral belt and parabelt rostral to thatborder. In contrast, the distribution of labeled cells associ-ated with the WGA-HRP (open triangles) and diamidinoyellow (open squares) injections, made caudal to the

border of AI and R, were generally spread across thelateral belt and parabelt caudal to that border. In case96-1L all of the injections were made rostral to the borderof AI and R. The distribution of labeled cells in this casewas almost entirely confined to the cortex rostral to theAI/R border. Similar patterns of rostrocaudal topographywere also observed in cases 94-64L (Fig. 4), 97-33L (Fig. 7),and 95-52L (Fig. 8).

There were two important exceptions to the rostrocau-dal trend. The first exception was found in an area withinthe circular sulcus (CiS) corresponding to part of themedial belt. An overlapping distribution of cells in theportion of the medial belt adjacent to core area R (i.e., RM)was labeled by all parabelt injections, whether caudal or

Fig. 4. Distributions of labeled neurons after injections of sixdifferent tracers in auditory belt cortex of the superior temporal gyrus(STG), case 94-64L. Injection sites (shaded ovals) contain symbols thatmark the locations of neurons labeled by tracers at the injection site(see key, upper left for tracers). Cortex of the left superior temporalregion has been unfolded, flattened, and cut parallel to the surface.The illustration is a composite of aligned sections through the depth of

the cortex. The core areas (rostrotemporal area [RT], rostral area [R],and auditory area I [AI]) were defined architectonically. The outlinedmiddle temporal (MT) and medial superior temporal (MST) visualareas were defined architectonically, and are shown for reference.Dashed lines mark the depths and lips of the lateral sulcus (LS), thesuperior temporal sulcus (STS), and the fold of the temporal pole (TP).For abbreviations, see list.


rostral to the AI/R border (Figs. 4, 5, 8). In contrast,significant numbers of labeled cells were found in thecaudal part of the medial belt (adjacent to AI), only afterinjections in the parabelt caudal to the AI/R border.Likewise, labeled cells in the medial belt adjacent to RT(i.e., RTM) were primarily associated with injections ros-tral to the border of R and RT. For example, in case 95-10L(Fig. 5), labeled cells from all four injections were repre-sented in RM. In the medial belt adjacent to AI, cells werelabeled only from the two injections caudal to the border ofAI with R (i.e., WGA-HRP, open triangles; diamidinoyellow, open squares). The RTM area contained only cellsfrom the rostral fast blue (filled circles) injection. In case96-1L (Fig. 6), only the three most caudal injectionslabeled neurons in RM (i.e., diamidino yellow, open squares;fluororuby, open triangles; rhodamine green beads, filledsquares).

The second exception was found in the superior tempo-ral sulcus (STS) where labeled cells were typically found in

patches. In many of these patches labeled cells fromrostral and caudal divisions of the parabelt overlapped. Incase 94-64L (Fig. 4), cells labeled by the most rostralinjection (diamidino yellow, filled circles) overlapped withcells labeled by the most caudal injection (fast blue, opensquares) in patches located in the upper bank of the STS.Note that there were also isolated patches of cells labeledonly by diamidino yellow, suggesting that the fast blue anddiamidino yellow injection sites receive distinct patterns ofprojections from the STS. There were no labeled cellsassociated with the rhodamine green bead injection (filledtriangles) in these patches, and only a few cells werelabeled by the rhodamine red bead injection (open circles),probably due to poor transport of these tracers in this case.In case 96-1L (Fig. 6), a large patch of cells located in theupper bank of the STS, in line with R, contained labeledcells from all five injections. A larger patch, located ros-trally contained labeled cells from all but the green beads(filled squares) injection. Other patches in the STS only

Fig. 5. Distributions of labeled neurons after injections of four different tracers in macaque monkey95-10L. The intraparietal sulcus (IPS) is included. For abbreviations, see list.


contained labeled cells associated with injections thatwere closely spaced. In addition to patches of overlappinglabel, the most rostral injections also resulted in isolatedpatches of labeled cells in the STS and rostral STG.

In two cases, parabelt injections were placed in extremecaudal or rostral positions relative to the core. In case94-64L (Fig. 4), the fast blue (open squares) injection wasplaced caudal to belt areas CL and CM. The resultingdistribution of labeled cells was atypical of injections in theparabelt. Patches of cells extended caudally to the edge ofthe section (i.e., intraparietal sulcus). A few cells werelabeled in the medial belt adjacent to R, but a greaternumber of labeled cells were found in the floor of thecaudomedial circular sulcus spreading into the insula.Only an occasional cell was labeled in the lateral belt orparabelt rostral to the injection site. Otherwise, labeledcells were found in patches overlapping with other tracersin the STS. In contrast, the adjacent rostral fluororuby

injection (filled squares) resulted in a distribution typicalof other parabelt injections. In case 96-1L the fast blue(filled circles) and rhodamine red beads (filled triangles)injections were placed in the STG rostral to the parabeltauditory cortex corresponding to superior temporal re-gions Ts1 and Ts2 of Pandya and Sanides (1973). Thedistribution of labeled cells on the STG remained largelywithin the cortex surrounding the injection sites anddid not label cells in the cortex lateral to the core region.There were no labeled cells in the medial belt adjacent toR, but large numbers of cells were found in the circularsulcus rostral to the tip of the core region. Otherwise,patches of cells were found in the upper bank of the rostralSTS and temporal pole. Because of this pattern of connec-tions, it is likely that these sites were rostral to theparabelt region.

The laminar distribution of labeled cells was examinedin case 95-52 (Fig. 8), which was cut in the coronal plane.

Fig. 6. Distributions of labeled neurons after injections of two tracers (FB and RB) in cortex judged tobe rostral to the parabelt region and three tracers (GB, FR, and DY) in the parabelt, case 96-1L. Auditorycore and belt areas were defined architectonically (see Fig. 2). For abbreviations, see list.


In the belt and parabelt regions, the heaviest concentra-tion of labeled cells was found in layers III and V (Fig. 9).Labeling in layer II was moderate and only scattered cellswere found in layer VI. Layer IV was usually devoid oflabeled cells. Recall that injections which encroached onthe lateral belt resulted in cell labeling in the core. A faintband of WGA-HRP-labeled cells was apparent in layer V ofAI in the core after such an injection (Fig. 9C). A fewlabeled cells are visible in layer III.

DISCUSSION

Over the last several years, the organization of auditorycortex in primates has been studied more intensively, andevidence has begun to emerge for a general pattern of

organization that divides auditory cortex into three re-gions: (1) core (primary cortex), (2) belt (secondary cortex),and (3) parabelt (association cortex). In this study, theregional ipsilateral cortical connections of the parabeltauditory cortex are described in macaque monkeys usingstandard neuroanatomical techniques (i.e., retrograde trac-ers, histochemical staining, immunocytochemical stain-ing, cytoarchitectonic analysis). Overall, our results indi-cate that the parabelt region has strong topographicconnections with the auditory belt region surrounding thecore, but not with the core itself. In addition, rostralsubdivisions of the auditory belt and parabelt are stronglyinterconnected, as are the caudal areas, whereas connec-tions between rostral and caudal areas are relativelyweak. These results are discussed in detail below with

Fig. 7. Distributions of labeled neurons after injection of one tracer (DY) in the belt-parabelt regionand two tracers (BDA, FB) in the parabelt, case 97-33L. For abbreviations, see list.


respect to the organization of known cortical auditoryareas in primates.

Architecture of the auditory core

The most reliably identified cortical auditory region inprimates is the core. In primates, the auditory core ex-tends caudorostrally along the surface of the superiortemporal plane. In the present study, the core regionstained darkly for myelin, acetylcholinesterase, and parv-albumin. In flattened sections, the darkly stained coreregion contrasted sharply with the surrounding cortex andwas easily identifiable. In coronal sections the transitionbetween the darkly stained layers of the core and morelightly stained layers of the surrounding belt cortex wasalso apparent, as described previously (Morel et al., 1993).Although the core has been variably subdivided, thelocation and estimated size of the core has been reasonably

consistent across studies (Fig. 10). The core is character-ized by a dense population of small granule cells especiallyin layers III and IV (e.g., koniocortex). The region isheavily myelinated and stains more darkly for cytochromeoxidase, acetylcholinesterase, and parvalbumin than thesurrounding areas (Morel and Kaas, 1992; Hackett et al.,1995; Jones et al., 1995). In New World owl monkeys, thecore has been subdivided into three primary or primary-like sensory areas: AI or auditory area I; R or the rostralarea; and RT or the rostrotemporal area (Morel and Kaas,1992). Two of these subdivisions (AI and R) have been alsorecognized in New World squirrel monkeys (Bieser andMuller-Preuss, 1992) and tamarins (Luethke et al., 1989).Previous studies of the auditory cortex in Old Worldmacaque monkeys have generally divided the auditorycore into just two subdivisions (i.e., AI and R), but an areahomologous to RT in owl monkeys has not been distin-

Fig. 8. Distributions of labeled neurons in a graphically unfolded surface view of the superior temporalregion (case 95-52L) reconstructed from a series of coronal sections. Injections of five tracers were placedin the parabelt, with some encroachment on the belt (DY, HRP, FB). Straight lines correspond to the planeof representative coronal sections. CiS, circular sulcus. For abbreviations, see list.


guished (Merzenich and Brugge, 1973; Burton and Jones,1976; Galaburda and Pandya, 1983; Morel et al., 1993;Jones et al., 1995).

The parcellation of the core into two areas has beenprimarily based on differences in patterns of tonotopicorganization, because the architectonic border between AIand R is subtle. Best frequency maps of the core inprimates indicate that AI and R are tonotopically orga-nized, but only AI has been shown to contain a completerepresentation of the frequency response of the cochlea.Higher frequencies are represented caudiomedially in AI,and low frequencies rostrolaterally; whereas in R lowfrequencies are represented caudolaterally and high fre-quencies rostromedially (Merzenich and Brugge, 1973;Imig et al., 1977; Aitkin et al., 1986; Luethke et al., 1989;Morel and Kaas, 1992; Morel et al., 1993). Thus, AI and Rshare a common low-frequency border. Morel and Kaas(1992) suggested that the tonotopic organization of RT in

owl monkeys may be opposite to that found in R (i.e., R andRT share a high-frequency border), but this conclusion wastentative, based on recordings from a limited number ofpenetrations in one case. The tonotopic organization of RThas not been investigated further.

In the present study, we used differences in stainingdensity to estimate the locations of borders between subdi-visions of the core. On this basis, three subdivisions of thecore, AI, R, and RT, were identified. The most caudalsubdivision, AI, was the largest, and stained more darklyfor parvalbumin, myelin, acetylcholinesterase, and cyto-chrome oxidase than R or RT. The location of this AI wascomparable with the AI depicted in several previousstudies (e.g., Merzenich and Brugge, 1973; Morel et al.,1993; Jones et al., 1995).

In nearly all primate studies, AI has been described asthe largest and most distinct subdivision of the core zone,occupying much of the caudal superior temporal plane.

Lateral Belt (ML) AI

A

C

B

Fig. 9. Example of an injection site and labeled neurons from a fastblue (FB) injection in case 95-52L (compare with Figure 8). A: The FBinjection site involves the belt and parabelt just lateral to auditoryarea I (AI). The diffusion zone of the tracer can be seen as a light regionaround the tissue damaged by injection. B: An adjoining Nissl-stained

sections showing the maximal damage at the FB injection site. C: Thedistribution of labeled neurons in AI and the adjoining lateral beltafter the FB injection. Note the sharp decrease in the numbers oflabeled cells from lateral belt to AI, especially in the superficial layers.For abbreviations, see list. Scale bar 5 1 mm in A,B, 0.5 mm in C.


Fig. 10. Schematics showing parcellations of the primate auditorycortex from current and previous investigations. In each panel,subdivisions corresponding to the auditory core are the most darklyshaded. The auditory belt subdivisions surrounding the core aredemarcated by the lighter shading. The parabelt and other regions

adjacent to the core on the superior temporal plane gyrus are notshaded. Borders between subdivisions are indicated by thin solid lines.Kam, koniocortical region, medial; Kalt, koniocortical region, lateral.For abbreviations, see list.


However, differences in the depicted size of AI do exist. In awidely cited study of auditory cortex in M. mulatta,Pandya and Sanides (1973) identified a relatively largekoniocortical region, composed of medial (Kam) and lateral(Kalt) divisions (see Fig. 10). In a subsequent modificationof that study, Galaburda and Pandya (1983) combinedKam and Kalt into a single koniocortical area (i.e., KA),and medial and lateral subdivisions of the koniocorticalzone (i.e., Kam and Kalt) have not been described in otherprimate studies. Based on its length in the rostrocaudaldimension, KA appears to correspond to AI and R identi-fied in this study and others (e.g., Merzenich and Brugge,1973; Burton and Jones, 1976; Morel et al., 1993; Jones etal., 1995). In the present study, AI averaged 10 to 12 mm inlength and 6 to 10 mm in width.

In more recent studies involving M. mulatta, M. nemes-trina, M. fascicularis, and M. fuscata, the estimated size ofAI ranged from 8- to 12-mm long in the rostrocaudaldimension and 4- to 6-mm wide medial-to-lateral (Morel etal., 1993; Jones et al., 1995). The results of these studiesdiffer substantially from an earlier study of M. mulattaand M. arctoides by Merzenich and Brugge (1973) in whichphysiologically defined AI averaged 4 to 6 mm in bothdimensions. Careful inspection of their data suggest thatthe smaller size of AI may have been the result ofincomplete mapping caudomedially in AI where frequen-cies above 20 kHz are likely to be represented. Heffner andHeffner (1989) obtained behavioral hearing thresholds inJapanese macaques up to 32 kHz, but they may besensitive to even higher frequencies. In the study byMerzenich and Brugge (1973) only three AI penetrationsin one case (70-142) were reported for which best frequen-cies exceeded 20 kHz (i.e., 21, 25, and 32 kHz). By usingthese penetrations as markers, the length of AI could havebeen extended to at least 8 mm, which is a length morecompatible with the results of other studies.

In our material, R was smaller than AI and also staineddarkly for parvalbumin, myelin, and acetylcholinesterase.In M. mulatta, R averaged 10 mm in length and tapered inwidth from 4-mm caudally to 2- or 3-mm rostrally. In M.nemestrina, R averaged about 8 mm in length tapering inwidth from about 4-mm caudally to 2- or 3-mm rostrally.The description of R across studies has been somewhatmore variable than AI with respect to its size and location.The border between AI and R is most reliably determinedfrom a reversal in tonotopic organization at the border.Based on responses to pure tones, Merzenich and Brugge(1973) estimated the size of R in M. mulatta and M.arctoides to be 3 to 4 mm in both dimensions. In M.fascicularis, Morel et al. (1993) established a borderbetween AI and R by a reversal in tonotopic organization.The lateral, medial, and rostral borders of R were based onthe relationship of the tonotopic map with architectonicboundaries. R averaged about 10 mm in length, tapering inwidth from about 4 mm caudally to about 2 mm rostrally.Somewhat smaller dimensions for R, based on cytoarchitec-ture and differential staining densities for parvalbuminand cytochrome oxidase, were reported by Jones et al.(1995) for M. fuscata. In brain sections cut parallel to theflattened cortical surface, R averaged about 8-mm long and2- to 3-mm wide. In M. fascicularis, however, the auditoryregion was reported to be much smaller overall than M.fuscata. Unfortunately, it was not possible to estimate thedimensions of R in M. fuscata from the images published intheir paper. However, comparison of photomicrographs of

coronal sections from Morel et al. (1993) and Jones et al.(1995) indicates that the identification of R can differ.Whereas Morel et al. (1993) labeled the darkly stainedouter bank of the circular sulcus as part of the coresubdivision R (their Fig. 5d–f), Jones et al. (1995) labeledthe same region as A-m, a belt subdivision that lies rostralto R in their material (their Fig. 10a–c). The gross anatomyand architecture of this region of cortex was remarkablysimilar in both studies, yet the cortex was assigned todifferent fields. Whereas the validity of R as a subdivisionof auditory cortex seems established, a consistent descrip-tion of its architecture and physiology has not beenaccomplished.

In addition to R, we observed what may be a third, morerostral subdivision of the core, RT, which occupies theouter bank of the circular sulcus (Figs. 2, 3, 10). In ourmaterial this putative subdivision was smaller than R andmost apparent in M. mulatta. In M. nemestrina, the regioncorresponding to RT was not as well differentiated, particu-larly in flattened sections. RT tended to stain more lightlyfor parvalbumin, myelin, and acetylcholinesterase than AIor R, but more darkly than the surrounding cortex. Cyto-chrome oxidase levels were less than AI and R, and notnotably different from that of surrounding cortex.

Based on size, location, and architecture, the area wedesignate as RT appears to be coextensive with paAr ofPandya and Sanides (1973). Indeed, these investigatorsstated that paAr ‘‘represents that parakoniocortex whichat first sight in cytoarchitectonics resembles the koniocor-tex the most.’’ Granular cell density in the upper layers ofpaAr was slightly reduced and myelination was weakercompared with Kam and Kalt, but greater than in thesurrounding areas. Thus, paAr resembled the koniocorti-cal core (Kam, Kalt) more than the other parakoniocorticalareas that surround the core (i.e., paAc, paAlt). Thisdescription is consistent with the architecture of RT asrevealed by parvalbumin, acetylcholinesterase, myelin,and Nissl staining in our material. Area paAr, like our RT,was identified in M. mulatta. In the study of Burton andJones (1976), the area we designated as RT may corre-spond to the small area they defined as RL in M. mulatta.AI of Burton and Jones (1976) encompassed a large regionon the supratemporal plane that appears to correspond toour AI and R; thus, their RL most likely corresponds to ourRT. Morel et al. (1993) made reference to RT in theirreconstructions, but made no attempt to define the bordersof RT in M. fascicularis. RT also appears to correspond tothe belt area A-m of Jones et al. (1995) discussed in moredetail in a later section.

Whether RT should be considered part of the core maybe best determined by examination of its connectionpatterns and physiologic properties, which are largelyunknown. Most of what is known about RT comes from asingle study in owl monkeys (Morel and Kaas, 1992). Inthese monkeys the tonotopic gradient in R appears toreverse rostrally, at the border with RT; however, RT hasnot been mapped in detail in any primate. In owl monkeys,RT is koniocellular in appearance and heavily myelinated,but less densely than AI and R, consistent with thefindings in M. mulatta. RT is interconnected with AI andR, but connections with other areas have not been reliablydetermined. In the present study, labeling in RT, as in AIand R, was conspicuously light after parabelt injections,which is a further argument for including RT in the coreregion. Because of architectural and connectional similari-


ties between AI, R, and RT, we included RT as a subdivi-sion of the core. RT was less obvious in M. nemestrina inour material, and RT may be variably differentiated inother species of macaques, as well. This might explain theinconsistent identification and assignment of RT.

Architectural differences between the subdivisions ofthe core are subtle and difficult to detect, particularly incoronal sections. Most studies (e.g., Pandya and Sanides,1973; Burton and Jones, 1976; Galaburda and Pandya,1983, Morel et al., 1993) have relied on coronal sectionsstained to reveal cell bodies and, less often, acetylcholines-terase or cytochrome oxidase patterns. Borders betweensubdivisions are roughly parallel to the coronal plane.Thus, it is not surprising that the putative subdivisions ofthe core have not been often identified solely on the basis ofarchitecture. In parasagittal sections and sections cutparallel to the surface of the superior temporal plane (e.g.,Jones et al., 1995), the subdivisions of the core are moreobvious because the core is elongated along the rostrocau-dal axis and borders are contained within the brainsections. In our material, subdivisions of the core weremost obvious in those sections of well-flattened cortex thatran parallel to lower layer III and layer IV throughout theentire core region.

Connections of the auditory core

Injections of retrograde tracers into the core suggestthat each subdivision has a similar, but unique, pattern ofcortical and thalamocortical connections. Both AI and Rreceive dense thalamic projections from vMGN, withsparser inputs to layer I from mMGN (Mesulam andPandya, 1973; Forbes and Moskowitz, 1974; Burton andJones, 1976; Fitzpatrick and Imig, 1978; Aitkin et al.,1988; Luethke et al., 1989; Morel and Kaas, 1992; Morel etal., 1993; Pandya et al., 1994; Hashikawa et al., 1995;Molinari et al., 1995). The strong connections between thevMGN and core are consistent with the observation in thisstudy, and others (Jones and Hendry, 1989; DeFelipe andJones, 1991; Hashikawa et al., 1995; Rausell and Jones,1991a,b; Rausell et al., 1992; Jones et al., 1995; Molinari etal., 1995), that both of these regions stain darkly forparvalbumin. Parvalbumin immunoreactivity is consid-ered to be a marker for the thalamocortical relay cells ofthe vMGN, and cells with high firing rates, in general(Kawaguchi et al., 1987; Heizmann et al., 1990).

The cortical connections of the core appear to be re-stricted to adjacent subdivisions within the core and thebelt of surrounding cortex (Merzenich and Brugge, 1973;Imig et al., 1977; Fitzpatrick and Imig, 1980; Brugge,1982; Galaburda and Pandya, 1983; Aitken et al., 1988;Luethke et al., 1989; Morel and Kaas, 1992; Morel et al.,1993; Jones et al., 1995). Each subdivision of the core ismore strongly connected with the immediately adjacentbelt subdivision; whereas connections with nonadjacentsubdivisions of the belt appear to be weaker. In owlmonkeys and macaques, strong connections exist betweenAI and the adjacent belt subdivisions (e.g., CM, CL, andML), whereas, weaker connections join AI with the morerostral belt areas, AL and RM, adjacent to R (Fitzpatrickand Imig, 1980; Galaburda and Pandya, 1983; Morel andKaas, 1992; Morel et al., 1993). A similar pattern ofconnections has been identified in marmosets (Aitkin etal., 1988; Luethke et al., 1989). R has strong connectionswith adjacent areas AL and RM, sparse connections withCM, ML, and RTL, and few or no connections with the

parabelt region (present results). RT does not appear tohave connections with AI, as an injection into RT of owlmonkeys labeled cells in R, but not AI (Morel and Kaas,1992). RT was also strongly connected with the subdivi-sions of the belt adjacent to R, but not the parabelt region(Morel and Kaas, 1992). In M. mulatta, an injection intopaAr (possibly RT) labeled cells in rostral KA (correspond-ing to R), but not caudal KA (corresponding to AI) (Cipol-loni and Pandya, 1989). Jones et al. (1995) illustratelabeled neurons in R and AI after an injection in A-m(possibly RT).

The results of the present study indicate that the core isnot significantly connected with the auditory parabeltcortex or adjacent regions of the superior temporal gyrus(Figs. 10, 11). However, when injections encroached uponthe lateral belt, substantial numbers of labeled cells werefound in the core. In these instances (Figs. 7–9), thedistribution of labeled cells was densest in the part of AIadjacent to the subdivision of the lateral belt (ML) invadedby the injections. Otherwise, only a few scattered cellswere labeled in the core, most often in R and RT. Injectionsin the parabelt also did not label neurons in the ventraldivision of the medial geniculate body (unpublished per-sonal observations).

Several previous studies produced quite similar results.Pandya and Sanides (1973) reported that lesions of paAlt,corresponding in position to the parabelt, in M. mulatta(cases 3 and 4) resulted in only limited degeneration ineither Kam or Kalt (corresponding to AI and R), and lightlabeling in paAr, corresponding to RT. In contrast, densedegeneration was observed in the medial belt and lateralbelt areas rostral and caudal to the lesions. Likewise,Galaburda and Pandya (1983) found that injections lim-ited to the gyral cortex of the STG of M. mulatta did notlabel cells in KA or paAr. However, injections of the STG,which also involved the belt cortex of the superior tempo-ral plane, labeled cells throughout the core. Similar pat-terns were observed by Cipolloni and Pandya (1989) andMorel et al. (1993). In owl monkeys, Morel and Kaas (1992)made two HRP injections lateral to the core. One injection(case 89-4), just lateral to R in the belt area AL, labeledpatches of cells throughout the core and STG. The otherinjection (case 89-45), made about 2.5-mm lateral to AI,labeled patches of cells across the STG rostral and caudalto the injection, but not within the core. From theseresults, the authors concluded that the lateral belt extendsonly 2 to 3 mm from the lateral edge of the core, a value inagreement with the present results.

Architecture of the auditory belt

The auditory core is flanked on all sides by a narrow beltregion (secondary auditory cortex). The appearance of thebelt is not homogeneous, suggesting that subdivisionsexist, but only limited physiologic data are available tohelp divide this cortex. Like the core, the belt has beenvariably subdivided into several areas in primates (Fig.10).There are a number of histologic distinctions between thecore and the belt, but the magnitude of the differencesvaries with the border region and the staining procedure.In general, belt areas are more similar in appearance tocore areas than is parabelt cortex. Thus, even the distinc-tion between core and belt is sometimes made with diffi-culty. Nevertheless, studies combining anatomy and physi-ology have identified several auditory representationswithin the belt region in the macaque monkey (Merzenich


and Brugge, 1973; Brugge, 1982; Morel et al., 1993;Rauschecker et al., 1995, 1997) and other primates (Imiget al., 1977; Aitkin et al., 1986; Morel and Kaas, 1992).Neurons in the belt respond to auditory stimulation, andat least parts of the belt appear to be tonotopicallyorganized. However, neurons in the belt are often difficultto drive with pure tones. The neurons tend to be broadlytuned, and respond less robustly with longer latenciesthan cells in the core (Merzenich and Brugge, 1973; Pfingstand O’Connor, 1981; Morel and Kaas, 1992; Morel et al.,1993; Rauschecker et al., 1995, 1997). The limited map-ping data suggest that tonotopic organizations of beltfields match the tonotopic gradients in the adjacent subdi-vision of the core, but further studies will be required toverify this conclusion.

The subdivisions of the belt proposed in the presentaccount relate to several previous schemas for parcelingthe region. Most notably, Pandya and Sanides (1973)identified three parakoniocortical areas surrounding thekoniocortical areas Kam and Kalt based on cyto- andmyeloarchitecture (i.e., proA, medial; paAlt, lateral; andpaAc, caudal) (see Fig. 10). Just caudal to the core, Pandyaand Sanides (1973) recognized the parakoniocortical areapaAc, bordered by reIt medially and Tpt laterally. In theirmaterial, paAc resembled the core cytoarchitectonically,except in the lower layers, and was heavily myelinated,but not as intensely as the core. Their description of paAcis fairly consistent with our observations in this region. InM. mulatta, we found that the cortex caudal to AI on thesuperior temporal plane stained darkly for parvalbumin,myelin, and acetylcholinesterase (Fig. 2). We subdividedthis region further into CM (after the caudal medial area of

Merzenich and Brugge, 1973) and CL, based on slightdifferences in their appearance in flattened sections, butthis conclusion remains tentative. In M. nemestrina thearchitectonic appearance of the region was more uniformand there were no clear differences between CM and CL.Numerous other studies have also described a subdivisionof cortex just adjacent to AI. Merzenich and Brugge (1973)distinguished large caudal and caudomedial regions fromAI on the basis of cytoarchitecture and physiology, andlabeled the entire region CM. In owl monkeys Morel andKaas (1992) identified the caudal cap of AI as a single area,C, based primarily on the connections associated with oneinjection involving AI and C. Medial to AI, however, was alarge densely myelinated area that they labeled CM. Asimilar description of CM in M. fascicularis was providedby Morel et al. (1993), but architectonic descriptions of Cwere not given. The distinction between C and CM in thatstudy was made primarily on the basis of connections, anda border between these fields was not specified. Jones et al.(1995) parceled the belt region capping AI caudally into asingle area, P-m, encompassing C and CM of Morel et al.(1993). In sections of flattened cortex processed to revealcytochrome oxidase and parvalbumin in M. fuscata, stain-ing in P-m was uneven, but there was no significantevidence for further subdivisions of the region based on thearchitecture in the material presented.

The belt cortex lateral to the core also has been variouslydivided into a number of areas. In the early study ofPandya and Sanides (1973) only a single, large region,paAlt, was distinguished along the entire lateral border ofthe core, and this area also extended laterally onto thesurface of the STG (Fig. 10). In their description, paAlt is

Fig. 11. A summary of auditory cortex subdivisions and connections based on the present and previousstudies. Double arrows indicate evidence for reciprocal connections. Heavy arrows indicate strongconnections and thinner arrows denote weaker connections. H, high-frequency stimuli; L, low-frequencystimuli; WB, wide band stimuli. Compare with Figure 10. For abbreviations, see list.


bordered laterally and rostrally by Ts3, which also borderspaAr laterally and rostrally on the superior temporalplane. This description of the lateral belt differs substan-tially from more recent parcelations of this region inseveral respects. Most notably, recent studies have ex-tended the lateral belt either just to the edge of the lateralsulcus (Merzenich and Brugge, 1973; Jones et al., 1995) orslightly beyond (Burton and Jones, 1976; Jones and Bur-ton, 1976). In Morel et al. (1993), the lateral belt extendsless onto the STG in the photomicrographs of coronalsections than in the summary drawings. Although Pandyaand Sanides (1973) depicted only one large lateral ‘‘belt’’area (paAlt) in their summary drawings, they did observesignificant differences in cytoarchitecture and myelinationbetween the portion of paAlt confined to the superiortemporal plane and the portion that extends onto the STG.In our material, staining for parvalbumin, myelin, acetyl-cholinesterase, and cytochrome oxidase was generallymore intense in the lateral belt confined to the supratempo-ral plane compared with the parabelt region of the STG.On this basis we estimate that the width of the lateral beltis no more than 3 to 4 mm in M. mulatta and M.nemestrina. If the lateral belt extends onto the STG at all,it is more likely to occur caudally, in ML and CL, where thecore occupies more of the surface of the superior temporalplane.

Studies in which the core has been subdivided into AIand R (and RT) also subdivided the lateral belt accordingly(Fig. 10). That is, separate areas are assigned to the beltcortex adjacent to AI, R, and RT. In owl monkeys, Moreland Kaas (1992) parcelled the lateral belt into three areas:PL, adjacent to AI; AL, adjacent to R; and LRT, adjacent toRT. Morel et al. (1993) identified PL and AL, adjacent to AIand R, respectively. In Merzenich and Brugge (1973), theirarea L bordered most of AI laterally, whereas area bbordered RL laterally and rostrally. In the present studythe cortex lateral to AI (ML) stained more darkly forparvalbumin, myelin, and acetylcholinesterase than thecortex lateral to R (AL).

Concepts of how the medial belt should be parcelledhave also varied. Pandya and Sanides (1973) identifiedthree medial areas: reIt, adjacent to paAc; proA, adjacentto Kam; and paI, adjacent to paAr. However, Burton andJones (1976) recognized a single area (Pi) medial to theirAI and RL, corresponding to Kam and paAr of Pandya andSanides (1973). A similar region, a, was depicted byMerzenich and Brugge (1973) as extending from AI tobeyond RL. Morel et al. (1993) identified two medial beltareas: CM, adjacent to AI, and RM, adjacent to R. Jones etal. (1995) proposed that A-m borders R medially, rostrally,and laterally (to the rostral border of L); thus their R iscapped by a single area, A-m. In owl monkeys, Morel andKaas (1992) subdivided the medial belt into three areas;the lateral belt, CM, adjacent to AI, RM, adjacent to R, andMRT, adjacent to RT. Similar subdivisions were proposedfor macaques (Morel et al., 1993). In our material, wefound little architectonic evidence for subdivisions of themedial belt. Staining in flattened sections was patchy anddid not correlate well between cases. Our decision topropose three medial belt subdivisions was based primar-ily on the pattern of connections observed with the para-belt cortex (discussed below). Therefore, like Morel et al.(1993), we recognized a distinction between CM and RM,adjacent to AI and R, respectively. We also propose thatRTM, adjacent to RT, differs from RM in connections, in

agreement with the architectonic separation of proA frompaI by Pandya and Sanides (1973).

Connections of the auditory belt

One of the principal findings of the present study, withrespect to the belt region, was that parabelt injectionscaudal to the border of AI with R densely labeled belt areascaudal to this border, with only weaker labeling rostrally;whereas, injections rostral to the AI/R border primarilylabeled cells in the belt rostral to that border with weakerlabeling caudally. These observations are consistent withthose from a number of studies that suggest the lateralbelt tends to interconnect most densely with immediatelyadjacent portions of the core and the parabelt. Thus,injections into AI in tamarins (Luethke et al., 1989)resulted in dense foci of label in the adjacent belt cortex,with notably fewer labeled cells in the belt cortex adjacentto R. In owl monkeys (Morel and Kaas, 1992), the rostrocau-dal topography was particularly evident when injectionswere confined to the lateral belt and did not involve thecore. For example, a fast blue injection in the belt cortexlateral to RT primarily labeled cells in the core rostral tothe border of R and RT, whereas an HRP injection lateralto AI produced no labeled cells beyond the border of R andRT. Similar results have been observed in macaque mon-keys. Galaburda and Pandya (1983) described a fairlyrobust rostrocaudal pattern in their material, althoughtheir injections were generally quite large, involving mul-tiple subdivisions of cortex. At each rostrocaudal level,adjacent subdivisions of the core and surrounding cortex ofthe belt (lateral belt) and root (medial belt) were found tobe more strongly interconnected than areas positionedmore rostrally or caudally. However, in a subsequent studyin M. mulatta, Cipolloni and Pandya (1989) reportedstronger connections between nonadjacent areas thanGalaburda and Pandya (1983). The authors stated that‘‘relatively restricted injections’’ allowed them to elaborateon the earlier study. The more recent data of Morel et al.(1993), Jones et al. (1995), and the present study lendsupport to the earlier conclusions of Galaburda and Pan-dya (1983), which suggested that stronger connectionsexist between areas at the same rostrocaudal level.

In our data there was one clear exception to the rostro-caudal trend of areal connections. In the medial belt cortexadjacent to R, corresponding approximately to RM, cellsprojected diffusely to sites all along the rostrocaudalextent of the parabelt, within the rostral and caudal polesof the auditory belt (Figs. 10, 11). This observation distin-guished RM from the other medial belt subdivisions (RTMand CM) and provided evidence that the rostral and caudallimits of the parabelt coincide with those of the belt.

Another major finding of the present study was thatinjections into the parabelt auditory cortex on the STGdensely labeled large numbers of cells in the belt, but notin the core. Only when an injection encroached upon thebelt cortex on the supratemporal plane were substantialnumbers of labeled cells found in the adjacent subdivisionof the core. This pattern of projections lends strong supportto the hypothesis that there is a narrow belt of cortexsurrounding the core, which mediates the flow of informa-tion between the primary auditory region and higher-orderassociation areas on the STG. This finding is consistentwith several previous observations. Pandya and Sanides(1973) made lesions involving paAlt in two cases (i.e., 3and 4). In case 3, the lesion involved the cortex of the STG


and planum temporale lateral to the core. Most of thedegenerating terminals were found rostrally and caudallyin the lateral belt and ‘‘stopped sharply at the border ofKalt, except that degenerated terminals continued into thesuperficial layers I and II of the koniocortical areas, Kamand Kalt.’’ In case 4, the lesion was smaller and confined tothe exposed STG. In this case, there were ‘‘no degenera-tions at all in Kam and Kalt.’’ In addition, several subse-quent connectional studies of the auditory cortex in pri-mates have included one or two injections in the parabeltregions that produced little or no label in the core (Gala-burda and Pandya, 1983; Cipolloni and Pandya, 1989;Morel and Kaas, 1992; Morel et al., 1993).

In summary, most results support the conclusion thatthe core is surrounded by a narrow belt of cortex, 2- to4-mm wide, which is bound medially by the insula anddoes not extend laterally beyond, or much beyond, the edgeof the lateral sulcus. Proposed subdivisions (Figs. 10, 11)within the lateral and medial belt are aligned with adja-cent core subdivisions; that is, borders between rostral andcaudal subdivisions of the core (i.e., AI/R, R/RT) extendmedially and laterally to subdivide the belt. The rostraland caudal poles of the belt are capped by subdivisionsthat join the lateral and medial belts. Based on theassumption that there are three subdivisions of the core inM. mulatta (AI, R, RT), the subdivision of the surroundingbelt regions might be organized into eight areas positionedaccording to the above criteria (Fig. 10). According to thismodel, adjacent subdivisions of the core and belt arestrongly interconnected; whereas, weaker connections arefound between nonadjacent areas.

Architecture of the auditory parabelt

A third region of auditory cortex occupies the dorsalsurface of the superior temporal gyrus, just lateral to theauditory belt (see Figs. 10, 11). This region, known as theparabelt, corresponds most closely to part of area 22 of themacaque and human brains (Brodmann, 1909). The para-belt is generally considered to be a higher-order auditoryregion or auditory association cortex (Pandya et al., 1969;Jones and Powell, 1970; Merzenich and Brugge, 1973;Mesulam and Pandya, 1973; Pandya and Sanides, 1973;Trojanowski and Jacobson, 1975; Chavis and Pandya,1976; Galaburda and Pandya, 1983; Markowitsch et al.,1985; Moran et al., 1987; Cipolloni and Pandya, 1989;Gower, 1989; Morel and Kaas, 1992; Morel et al., 1993;Rauschecker et al., 1995), a conclusion that is consistentwith the results of a number of ablation-behavioral studies(Cowey and Weiskrantz, 1976; Wegener, 1976; Costalupes,1984; Creutzfeldt et al., 1989; Colombo et al., 1990).Compared with the core and belt regions, anatomical andphysiologic data concerning the superior temporal regionare very limited. In the present study, the belt regionoccupying the superior temporal plane stained much moredensely for acetylcholinesterase, cytochrome oxidase, my-elin, and parvalbumin than the parabelt region on theexposed superior temporal gyrus. Cells in the parabeltcortex appeared to be less densely packed and they demon-strated a stronger tendency to be arranged in verticalcolumns than cells in the lateral belt. The architecturaland connectional data discussed further below stronglysupport our distinction between the belt and parabelt.

The most widely cited parcelations of the macaquesuperior temporal gyrus, based on architectural and con-nectional evidence, are those of Pandya and Sanides (1973)

and Galaburda and Pandya (1983; see Fig. 10). As dis-cussed earlier, their koniocortical area, KA, appears to becoextensive with our AI and R, whereas their parakoniocor-tical area paAr, may correspond to our RT. Although theseinvestigators defined a medial belt region composed ofseveral subdivisions (i.e., the root zone), they made nospecific reference to a corresponding lateral belt; instead,several areas that occupy the cortex of the STG extend tothe lateral edge of the core encompassing both the lateralbelt and parabelt (i.e., Tpt, paAlt, Ts3, and Ts2). Neverthe-less, Pandya and Sanides (1973) observed architecturaland connectional differences between the gyral and pla-num portions of paAlt and Ts3, although they did notsubdivide these regions. The parcelation of Pandya andSanides (1973) was retained in subsequent studies with-out significant modification (Galaburda and Pandya, 1983;Cipolloni and Pandya, 1989). Other studies also providedevidence for an auditory parabelt region. Merzenich andBrugge (1973) included the parabelt region in their parce-lation of the auditory cortex, naming it ‘‘c’’ to distinguish itfrom their lateral belt areas (Fig. 10). Area T2, distin-guished by Jones and Burton (1976), involved much of thesuperior temporal gyrus adjoining the belt region, T1, andthe rostral planum temporale bordering the core area, RL(Fig. 10). In owl monkeys, Morel and Kaas (1992) observedarchitectural and connectional differences between thenarrow belt of cortex surrounding the core and the adja-cent parabelt region. In Jones et al. (1995) and the presentstudy, significant architectural differences, matching thoseof Pandya and Sanides (1973), were observed between theplanum and gyral regions of cortex lateral to the core.

With respect to differences in the rostrocaudal dimen-sion of the parabelt, Pandya and Sanides (1973) noted agradual increase in architectonic differentiation from ros-tral (Ts1) to caudal (Ts3) in the cortex of the superiortemporal gyrus. Specifically, they cited an increase ingranularization, improved differentiation of layers V andVI, and an increase in myelination from rostral to caudal.In our material, there was a gradual increase from rostralto caudal in the intensity of staining for acetylcholinester-ase, myelin, and parvalbumin, which was obvious acrossthe core, belt, and parabelt regions (Fig. 2). Although thistrend matches the topography of the connections observedin the present study, distinct borders between divisions ofthe belt parabelt were not obvious.

Physiology of the auditory parabelt

Neurons in the STG reportedly respond inconsistently tosimple acoustic stimuli such as pure tones (Gross et al.,1974; Leinonen et al., 1980; Rauschecker et al., 1995),whereas significantly greater responsiveness has beenfound by using spectrally complex stimuli, including spe-cies-specific vocalizations (Leinonen et al., 1980; Symmes,1981; Rauschecker et al., 1995; Tian and Rauschecker,1995). Rauschecker et al. (1995) examined the responseproperties of single neurons in the STG of rhesus macaquemonkeys to pure tones, bandpass noise, and species-specific vocalizations. In over 90% of the neurons re-sponses to bandpass noise and vocalizations were signifi-cantly enhanced compared with the responses evoked bypure tones (which often had little effect). In addition, mapsof best center frequency revealed a continuous rostrocau-dal progression, with two frequency reversals, suggestingthe presence of at least three functionally distinct areasalong the dorsal STG. In a related study, Tian and Raus-


checker (1995) found that neurons in this region respondselectively to specific FM rates and directions that matchthe FM fluctuations in monkey vocalizations. The resultsof these two studies are consistent with the hypothesisthat the parabelt region in macaque monkeys is primarilyinvolved in the analysis of complex auditory stimuli. Theproposed functional subdivisions of the STG in thesestudies roughly match our parcelation of the region basedon connections. Parts of the parabelt of the caudal superiortemporal gyrus may also participate in the multimodalprocessing of spatial and temporal information. This find-ing is not surprising given its proximity to somatosensoryand visual association cortices. For example, Leinonen etal. (1980) studied the responses of neurons in the caudalparabelt, corresponding to area Tpt, by using auditory,somesthetic, and visual stimuli. Almost all (96%) of cellsresponsive to auditory stimulation responded to spectrallycomplex sounds, including vocalizations. Furthermore, in62% of these units, responsiveness was clearly dependenton the angle of incidence of the sound source. Many cellswere responsive to somesthetic stimulation of the ear,neck, and shoulder, as well as rotation of the head. Threecells were only activated by moving visual stimuli, andmany units demonstrated bimodal responses to auditoryand somesthetic or auditory and visual stimuli.

Connections of the auditory parabelt

Previous ablation and tracer injection studies of connec-tions suggested that much of the dorsal superior temporalgyrus has auditory function (Pandya and Sanides, 1973;Galaburda and Pandya, 1983; Cipolloni and Pandya, 1989;Morel and Kaas, 1992; Morel et al., 1993). Thalamic inputto the parabelt is thought to arise primarily from themedial pulvinar (Locke, 1960; Trojanowski and Jacobson,1975; Burton and Jones, 1976; Streitfeld, 1980), which alsohas projections to visual and somatosensory cortical areas.Strong connections have also been found with the suprage-niculate, limitans, dorsal medial geniculate, and magnocel-lular medial geniculate nuclei (Hackett et al., 1996). Otherstudies, including results from the present cases, indicatethat the parabelt has connections with a number of areasin the frontal lobe (Jones and Powell, 1970; Chavis andPandya, 1976; Jacobson and Trojanowski, 1977; Barbasand Mesulam, 1981, 1985; Petrides and Pandya, 1988;Deacon, 1992; Morel and Kaas, 1992; Barbas, 1993; Hack-ett et al., 1997; Romanski et al., 1997), but a systematicdescription of these connections has not been published.

Our present findings indicate that the parabelt receivesstrong ipsilateral projections from the belt, parabelt, andsuperior temporal sulcus, but not the core (Fig. 11). Lessdense homotopic connections (not described) were foundwith the same regions in the opposite hemisphere. Rostro-caudal sequences of injections within the parabelt resultedin rostrocaudal distributions of labeled cells in the para-belt. Thus, connections within the parabelt were mostdense locally. The cortex of the superior temporal gyrusrostral to core area RT, corresponding approximately toTs2 (Pandya and Sanides, 1973), had denser connectionswith the cortex rostral to the border of R and RT. Similarly,isolated injections in the STG caudal to belt areas CL andCM, corresponding to Tpt (Pandya and Sanides, 1973),revealed connections with the caudal insula, caudal STG(Tpt), and STS, but few connections with the belt orparabelt lateral to the auditory core. Thus, the cortex ofthe dorsal STG between the rostral and caudal poles of the

auditory belt was preferentially and topographically con-nected with the cortex between those poles. We proposethat this region corresponds to the auditory parabelt.

The parabelt may be composed of as many as two orthree subdivisions that match subdivisions of the core andbelt (Figs. 10, 11). This finding is suggested by some of themore distant connections within the parabelt, as well aswith the belt. Our conclusions are consistent with severalobservations in earlier studies in which ablations orinjections were made in the parabelt region. In one mon-key, Pandya and Sanides (1973) confined a small lesion tothe gyral portion of paAlt. Dense concentration of degener-ated terminals were found rostrally and caudally and inthe belt cortex lateral to the core, but not within the core. Asecond lesion of paAlt, involving the planum temporale,resulted in heavy degeneration within paAlt and markedlyweaker degeneration within the core.

The findings of Galaburda and Pandya (1983) are alsosimilar to ours, although their injection sites were largerand fewer in number. Nonetheless, two injections re-stricted to the parabelt involving Ts3 and paAlt labeledcells in the medial and lateral belt regions, but not withinKA or paAr. Retrograde labeling was restricted primarilyto Ts3 and paAlt, and the rostral border of Tpt. Antero-grade terminal labeling involved much of Ts2, as well. Ourresults also compare favorably with those of Cipolloni andPandya (1989), who placed five injections in or around theparabelt in paAlt and/or Ts3 of four monkeys. In one casean injection made in the middle of the STG involving paAltand Ts3 labeled large numbers of cells in the cortexsurrounding KA and paAr, with lighter labeling in Tpt,Ts2, and Ts1, and no labeled cells in KA. PaAr was lightlylabeled. However, similar injections, apparently confinedto gyral paAlt, labeled cells in and around KA and paAr,including Tpt. The reason for the unexpected label in KA(AI and R) is unclear. Furthermore, the rostrocaudaltopography observed in the present study and that ofGalaburda and Pandya (1983) was not as apparent in theirdata. Most notably, an injection primarily involving paAr,labeled cells evenly over most of the superior temporalgyrus and plane, except for paAc, Ts1, and the temporalpole (Pro). Most of their other injections, however, resultedin a distribution of labeled cells skewed in the rostral orcaudal direction, depending on the location of the injection,consistent with the rostrocaudal topography.

Although there are minor discrepancies between stud-ies, the major conclusions of the present study seemwell-supported, particularly when one considers the num-ber of injections analyzed in our material. In five cases, wemade a total of 23 injections in the superior temporal gyruscorresponding to Tpt, paAlt, Ts3, and Ts2 (Pandya andSanides, 1973). The results across cases were highlyconsistent, and they also correspond to more limitedfindings of others (e.g., Pandya and Sanides, 1973; Gala-burda and Pandya, 1983; Morel and Kaas, 1992; Morel etal., 1993; Jones et al., 1995).

In summary, the superior temporal gyrus in macaquemonkeys is composed of several areas that are distinctfrom adjacent areas on the surface of the superior tempo-ral plane (Figs. 10, 11). The region described as theauditory parabelt in our results appears to correspond tothe gyral portion of areas paAlt and Ts3 of Pandya andSanides (1973). Taken together, the results of all availabledata suggest that the parabelt may contain at least twosubdivisions (CP, RP), which are strongly connected to


adjacent areas of the lateral belt (ML, AL, RTL) andnearby areas of the medial belt (RTM, RM, CM). Together,the centrally located core, surrounding belt, and adjacentparabelt region are sequentially interconnected, and theymay compose most of what can be called the ‘‘auditorycortex.’’ The STG cortex caudal to CP, known as Tpt(Pandya and Sanides, 1973), has weaker connections withthe auditory region and may not be strictly or predomi-nately auditory in function. Rostral to the auditory para-belt and belt cortex on the superior temporal plane,corresponding to Ts2, Ts1, and Pro (Pandya and Sanides,1973), are a number of areas with progressively weakerconnections with the auditory areas. Whereas Pandya andSanides (1973) concluded that ‘‘the rostral half of thesuperior temporal gyrus clearly lies outside of the auditoryregion’’ it only seems likely that these areas are progres-sively less devoted to audition as one moves rostrallytoward the temporal pole.

ACKNOWLEDGMENTS

This research was supported by National Institutes ofNeurological Disorders and Stroke grant NS 16446 toJ.H.K., and NIDCD Research Fellowship DC 00249 toT.A.H.

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subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex...

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