Proc. Nati. Acad. Sci. USAVol. 85, pp. 4914-4918, July 1988Neurobiology

Retinal afferent arborization patterns, dendritic field orientations,and the segregation of function in the lateral geniculatenucleus of the monkey

(intracellular recording/horseradish peroxidase)

CHARLES R. MICHAELDepartment of Cellular and Molecular Physiology, Yale Medical School, 333 Cedar Street, New Haven, CT 06510

Communicated by Irving T. Diamond, March 7, 1988

ABSTRACT Optic tract fibers and cell bodies in the lateralgeniculate nucleus of the monkey were studied intracellularlywith micropipette electrodes containing the marker enzymehorseradish peroxidase. Single optic-tract fibers always pro-jected to only one of the six geniculate layers. The majority ofthe axons innervating the four parvocellular laminae werered/green opponent color units; their terminations formedcylindrical columns that were perpendicular to the layers. Insimilar fashion, the geniculate cells in the parvocellular layerswere mostly red/green units with narrow, bipolar dendriticfields oriented normal to the laminar borders. The majority ofthe retinal axons ending in parvocellular layers 6 and 5 wereon-center units; nearly all geniculate cells in these two laminaewere also on-center neurons. In layers 4 and 3 most terminatingoptic-tract fibers, as well as the geniculate cells themselves,were off-center units. AU axons projecting to the magnocellularlayers were broad-band units with spherical terminal arbori-zations. The magnocellular geniculate neurons, which werealso broad band, had extensive spherical dendritic fields thatoften crossed laminar borders. Thus, the terminal patterns ofeach class of retinogeniculate axon closely resembled thedendritic orientations of the functionally related geniculatetarget cells.

The ganglion cells in the retina of the monkey consist ofseveral distinct functional classes (1). Nearly all ofthem haveon-center or off-center receptive fields. On-center ganglioncells discharge in response to an increase in the illuminationfalling on their receptive field centers, whereas off-centercells fire when the light level decreases. The field centers ofmany of these ganglion cells receive input from only one ofthe three cone classes; in turn, their surrounds are connectedwith only one of the two remaining cone types. As a result ofthese synaptic connections, the cells are excited by certaincolors and inhibited by others. Some ganglion cells havecenter/surround receptive fields but show no special interestin color; both their centers and surrounds receive summatinginputs from all three cone types. Consequently, these gan-glion cells have broad-band spectral sensitivities.Axons of the retinal ganglion cells project to the lateral

geniculate nucleus (LGN) in the thalamus. Here are found thesame functional classes seen in the retina, with no obviouschanges in their physiological properties (2-4). In the retinathe different ganglion cell types are often found next to oneanother, whereas in the LGN each functional class is ratherstrictly confined to certain layers. For instance, nearly allopponent color neurons are located in the four dorsal par-vocellular layers, whereas most broad-band cells are limitedto the two ventral magnocellular laminae (2, 4, 5). Within theparvocellular layers almost all neurons in laminae 6 and 5 are

on-center cells, whereas layers 4 and 3 contain mostlyoff-center neurons (4). This laminar separation of the genic-ulate-cell types must be due to the specific projectionpatterns of the retinal afferent axons (optic-tract fibers).With development of the combined technique of intra-

axonal recording and injection, it is now possible to examinethe terminal patterns of the various physiological classes ofretinal afferents to the LGN (6-8). In this study micropipetteelectrodes were used to record intracellularly from optic-tract fibers entering the LGN ofthe monkey. The axons werefunctionally characterized by a series of tests and were thenfilled iontophoretically with the marker enzyme horseradishperoxidase (HRP). Injection of the optic-tract axons pro-duced a Golgi-like stain of their terminal arborizations thatcould then be correlated with their receptive fields, chromaticproperties, and laminar location. The results provide evi-dence that the physiologically distinct classes of retinal affer-ent axons have different terminal patterns and laminar dis-tributions in the LGN of the monkey.

Cell bodies in the LGN were also studied with the sametechnique of intracellular recording and HRP injection. Theterminal patterns ofthe functionally characterized optic-tractfibers were then compared with the dendritic fields of thephysiologically identified geniculate neurons. The data revealthat the dendritic trees of each geniculate cell type match theshape of the terminal arbors of the retinal axons belonging tothe same functional class.

METHODSMethods used in these experiments were similar to thosedescribed in detail elsewhere (6, 7, 9). Cynomolgus monkeys(Macaca fascicularis) were anesthetized with halothane forthe surgical procedures, then paralyzed, and artificiallyrespirated with 70% N20/30% 02 during the experiment. Theanimal's head was held in a stereotaxic instrument; its bodyand limbs rested on a thick sponge-rubber pad. All pressurepoints and wounds were infiltrated with a long-acting localanesthetic (procaine). Body temperature was maintainedwith a hot-water heating pad. The corneas were fitted withcontact lenses, and the eyes were focused with supplemen-tary lenses on a tangent screen at a distance of 145 cm. Theanimal's heart rate, electrocardiogram, expired C02, andrectal temperature were monitored throughout each experi-ment. In the more recent experiments electroencephalogramand arterial blood pressure were also followed to furtherensure that the monkey was free of pain.

After opening the skull a saline-filled glass guard micropi-pette (7) was positioned 1-2 mm above the surface of theLGN. The recording micropipette was then lowered downthrough the guard to protect its tip and to guide its descent.

Abbreviations: LGN, lateral geniculate nucleus; HRP, horseradishperoxidase.

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Proc. Natl. Acad. Sci. USA 85 (1988) 4915

Micropipettes were made from 1.0-mm Omega Dot capillarytubing pulled to a taper of 25-30 mm. They were filled bycentrifugation with a solution of 200 mM potassium acetate(pH 6.8) containing 10% HRP (Sigma type VI). The tips werebroken to a resistance of 150-400 MU for axon recordings orbeveled to 80-120 MU for cell body experiments. When anaxon was impaled, its receptive field was located, the fieldcenter was mapped, the- center sign and ocularity weredetermined, and the electrode depth was noted. Responses towhite and monochromatic spots and annuli were recorded toclassify the axon's functional properties and to assign theaxon to a specific category. Cell bodies were examined in asimilar manner, except that the cells were characterizedwhile recording extracellularly, and then the soma was pene-trated and filled with HRP.

After a neuron had been studied physiologically, it wasfilled with HRP by passing positive dc current through theelectrode (3-10 nA for 1-10 min for axons; 2-5 nA for 1-5 minfor cell bodies). At the conclusion of the experiment, theanimal was perfused with 2% (wt/vol) glutaraldehyde and 1%(wt/vol) paraformaldehyde in 100 ,uM sodium phosphatebuffer (pH 7.2). The LGN was removed in a block, allowedto sink overnight in 30%6 sucrose, and then serially sectionedin the coronal plane at 80 AM on a freezing-stage microtome.Sections were developed for reaction product by use of di-aminobenzidine, cobalt chloride, and nickel ammonium sul-fate (10, 11). Filled axons and cells were reconstructed fromserial sections with a drawing tube attached to a LeitzOrthoplan microscope equipped with a x 100 oil-immersionobjective. Complete staining of an axon's arborizations or acell's dendritic tree was confirmed by tracing each branchingprocess to its ultimate ending in one or more darkly filledterminal boutons (axons) or beaded swellings (cells). Eitherthe boutons or the swellings could always be distinguishedfrom cut ends or fading processes.

RESULTSOptic Tract Fibers. Any individual optic-tract fiber pro-

jected to only one of the six geniculate layers (12). No fiberever sent branches to both a parvocellular and a magnocel-lular layer, nor did any axon end in a pair of parvocellularlaminae innervated by the same eye-i.e., layers 6 and 4 or5 and 3 (6, 7). Furthermore, all recovered fibers projectedonly to the LGN (6, 7). Single axons traced for severalmillimeters back into the optic tract did not appear to haveany branching processes. Perry and his collaborators (13, 14)have also reported that it was very rare to find retinoge-niculate axons that branched to innervate both the thalamusand the midbrain of the monkey. Nevertheless, because theoptic-tract fibers were always injected close to their entranceinto the LGN, it is possible that fine collaterals destined forthe midbrain were not backfilled with the HRP.

Optic-tract fibers destined for a parvocellular lamina (83axons) branched only after they entered the layer of termi-nation. At that point most of them (59 fibers) arborized in adirection primarily perpendicular to the borders ofthe lamina(7, 12). The terminal arbors usually reached across the entirewidth ofa layer but never extended into an interlaminar zone.The envelope of the boutons was approximated by a narrowcylinder, which was on the average -40,M wide. Theseaxons exhibited physiological properties that were typical ofa major class of cells (type 1) first seen in the LGN by Wieseland Hubel (2) and later found at the retinal ganglion cell levelby DeMonasterio and Gouras (1). This class had concentri-cally organized center/surround receptive fields with smallcenters (2-15'), gave sustained responses to prolonged lightstimulation, and exhibited red/green color opponency tomonochromatic stimuli (2-5, 15-17). Measurements with avariety of monochromatic stimuli indicated that the on- or the

off-center of a given fiber received inputs either from red- orfrom green-sensitive cones, whereas the surround responsewas mediated by the other cone type.Although their terminal patterns appeared very similar, the

on-center and the off-center optic-tract fibers had quiteseparate parvocellular destinations. Nearly all axons termi-nating in layers 6 and 5 were on-center (29 of 32), whereas themajority of those ending in layers 4 and 3 were off-center (23of 27). Schiller and Malpeli (4) have reported a similar dis-tribution for the geniculate cell bodies themselves. Thus thespecific projection patterns of the optic-tract fibers must bethe basis for the functional segregation ofthe geniculate cells.

Fig. 1 shows the terminal field of an HRP-filled axon thatended in parvocellular layer 6 and was driven by the contra-lateral eye. The axon rose to the top of the layer and thenturned and coursed downward, giving off numerous branchesas it descended; arborizations ran in a direction primarilyperpendicular to the laminar borders. The overall terminalfield was <35 1LM wide, but it extended across the full heightof the layer. There were many bouton swellings along eachbranch, as well as one at each termination. Density of theboutons was about the same across the laminar width.

Fig. 2 graphically illustrates the responses of this sameaxon to white, red, and green spots of increasing size. Theaxon's receptive field center was about 2' in diameter. Withwhite stimuli the fiber's field was on-center and off-surround;thus, the axon was insensitive to diffuse light. The strongeston response was to a spot about 2' in diameter (1/320) a 40spot had no effect. When monochromatic stimuli were used,the field center was most responsive to red spots, whichevoked on discharges, whereas the surround was mostsensitive to green annuli, which produced off responses. Theresponses to red spots larger than about 2' (1/32°) wereessentially equal, whereas the discharges for green spotsincreased to a stimulus diameter of about 40 and then leveledoff.

In addition to the red/green optic tract fibers, whichterminated in all four parvocellular layers, there were blue-on, yellow-off axons (21 units) that arborized only in layers4 and 3 (4). These axons had circular receptive fields thatlacked antagonistic surrounds. Terminations of one of thesefibers were always limited to either the upper or the lowerborder of a single layer. Three additional axons had sphericalarborizations, center/surround receptive fields, and broad-band spectral sensitivities. The functional and structuralproperties of these two classes of optic-tract fibers will bediscussed in a later paper.

6

FIG. 1. Coronal reconstruction of the arborization pattern of anoptic-tract fiber ending in parvocellular layer 6. The narrow terminalenvelope was perpendicular to the borders of the layer and was -35AuM wide. Injection site is indicated by the arrow pointing to theslightly swollen portion of the axon. The unit, which was driven bythe contralateral eye, was a red on-center, green-off surround fiber.Its field center was about 2' in diameter and was located 30' from thecenter of the fovea. Scale bar equals 100 ,uM.

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Proc. Natl. Acad. Sci. USA 85 (1988)

1

WHITE

RED

GREEN (OFF)

1/16 1/4 1 4 160

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FIG. 2. Area-response curves for the fiber in Fig. 1. White, red(660 nm), and green (520 nm) spots were centered on the receptivefield, flashed for 1-sec duration and increased progressively indiameter. The ordinate scale refers to the number of impulsesoccurring during the 1-sec flash for the white and the red stimuli andto the 1-sec period after the flash for the green spots. Each pointrepresents the average response for 10 stimulus presentations. Thescale on the abscissa is logarithmic. Response to white spots peakedat about 2' (1/320, arrow A); strong peripheral antagonism occurredwith larger stimuli. The response to increasingly bigger red spots rosevery rapidly and then plateaued at about 2' (1/320, arrow A). The offdischarge to green spots continued to increase to 40, at which pointthis response also leveled off (arrow B).

Branching patterns and terminal arborizations of the axonsending in the magnocellular layers (29 fibers) were distinctlydifferent from those of the opponent-color axons going to theparvocellular laminae. These fibers usually bifurcated sev-eral times at a considerable distance from their eventualdestination (7). The various branches of an axon often fol-lowed very circuitous paths, but they inevitably converged toa single terminal locus. Their terminal fields were large andspherical with a mean diameter of 125 AM; these fields oftenreached across the full width of a layer but never extendedinto an interlaminar zone.The axons terminating in the magnocellular layers were

also physiologically quite distinct from their parvocellularcounterparts. These axons had many functional characteris-tics of the Y ganglion cells in the monkey's retina (1). Theygave phasic responses to prolonged stimuli and were broad-band (non-opponent) in their responses to color. These fibershad concentric receptive fields with on- or off-centers thatwere generally larger (8'-20) than those of the axons ending inthe parvocellular laminae. Both on- and off-center axonsterminated in each of the two magnocellular layers; theseaxons did not differ obviously in their arborization patterns.

Fig. 3 illustrates the arborizations of an on-center, off-surround optic-tract fiber driven by the contralateral eye andterminating in magnocellular layer 1. The parent axon bifur-cated three times in the optic tract, but the four branchesterminated in the same area of the LGN. The terminal fieldwas radially symmetrical and about 130 AuM in diameter.Terminals extended across the entire width of the layer butdid not enter the interlaminar zone separating layers 1 and 2.As with the fibers ending in the parvocellular layers, boutonswellings occurred along the branches and at their termina-

FIG. 3. Arborization field of a broad-band on-center, off-surround fiber in magnoceliular layer 1. The unit was driven by thecontralateral eye. The parent axon branched several times in theoptic tract, but all terminals were confined to the same locus. Thelarge terminal envelope was roughly spherical with a diameter ofo130 AM. The receptive-field center was about 8' in diameter and 2°from the foveal center. Arrow, injection site. Scale, 100 AtM.

tions. The boutons were evenly spread across the width ofthelamina.

Fig. 4 shows the responses of this same fiber to increas-ingly larger white, red, and green spots. Small white spots inthe field center evoked transient on responses, whereas largeones produced no responses. Although not illustrated, whiteannuli elicited off discharges. Small monochromatic spotsalso yielded phasic-on discharges, regardless of the wave-length used. All color stimuli, as well as white, evoked

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FIG. 4. Responses of the axon in Fig. 3 to increasingly biggerwhite, red (650 nm), and green (540 nm) spots. Curves for all threestimuli were similar. Phasic on responses peaked for spots about 8'in diameter (1/8°, arrow) and then rapidly declined for bigger stimuli,indicating that peripheral antagonism was present at all wavelengths.Scale conventions as in Fig. 2.

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4916 Neurobiology: Michael

Proc. Natl. Acad. Sci. USA 85 (1988) 4917

maximum responses for a spot about 8' in diameter (1/80).Large spots of any color did not elicit a response, indicatingthat peripheral suppression was present at all wavelengthstested. Thus, the field center and surround seemed to havethe same broad-band spectral sensitivity. Consequently,unlike an opponent color unit, this fiber did not respond toeither long- or short-wavelength diffuse light.

Geniculate Cel Bodies. All cell bodies injected in theparvocellular and magnocellular layers had axons that passedup into the optic radiation, indicating that these neurons wererelay cells and not interneurons. Unlike some geniculocor-tical axons in the cat (9), these fibers never issued collaterals,either within or above the LGN. When a well-filled axoncould be traced out of the LGN and through the overlyingthalamic reticular nucleus, this fiber never gave off anybranches. However, some axons appeared faint at that dis-tance from their somas. Thus, these fibers could haveproduced fine collaterals unstained by the HRP.The dendrites of cells in the parvocellular laminae (77

units) were confined to the layer in which the soma waslocated. They never extended into an adjacent layer or eveninto an interlaminar zone. Most parvocellular neurons (50units) had dendritic trees that were oriented perpendicularlyto the borders of the layers, essentially along projection lines(9, 18-21); these dendritic trees averaged 100 gM in width.The parvocellular neurons with perpendicular dendritic

fields were red/green, center/surround opponent color units(2-5, 15-17). They appeared to have the same functionalproperties as their ganglion-cell counterparts in the retina (1).They had very small field centers (2'-15') under the influenceof either red or green cones; the surround response wasmediated by the other cone type. These neurons gave oneresponse, either on or off, to long-wavelength light and theopposite response to short-wavelength illumination. Thesecells always exhibited sustained discharges to prolongedstimuli. Consistent with the cell body results of Schiller andMalpeli (4) and the optic tract-fiber studies reported here,most neurons in dorsal parvocellular layers 6 and 5 wereon-center cells (24 of 27), whereas nearly all those in ventralparvocellular laminae 4 and 3 were off-center units (20 of 23).In spite of their rather strict segregation, the on- and theoff-center cells did not appear structurally different in anyobvious way.

Fig. 5 is a reconstruction of a red on-center, green off-surround cell found in layer 5. The cell is best described as abitufted bipolar neuron. The orientation of the dendritic field

was normal to the boundaries of the layer; the field reachedacross the lamina and was about 80 gM wide at its extremes.Even the cell body itself was elongated in a direction perpen-dicular to the layer. The soma was located near the middle ofthe lamina, and, consequently, the two dendritic poles wereabout equal in size. Note that no dendrites emerged from theleft or right side of the cell body. Thus the neuron wasprimarily contacted only by afferents terminating in the topand the bottom third of the layer. As with the terminals of theoptic-tract fibers, each dendritic branch had many beadedswellings along its length and always ended with one of thesedilatations. The axon left the soma from its dorsal aspect andtook a meandering course out of the LGN and into the opticradiation. The axon was traced for over 3 mm before it beganto fade, and it apparently gave off no collateral branches.The cell was driven by the ipsilateral eye and had a field

center -3' in diameter. The receptive field could be mappedwith very small white spots; large white spots had no influ-ence. Both small and large red spots elicited strong sustainedon responses, whereas increasingly larger green spots pro-duced greater inhibition and bigger off discharges. Althoughnot illustrated, the area-response curves for this cell weresimilar to those in Fig. 2 for the opponent-color optic-tractfiber.

Beside the red/green opponent-color neurons, there alsowere blue-on, yellow-offgeniculate cells (23 units). They hadcircular receptive fields with no surrounds, and their somaswere restricted to the borders of layers 4 and 3 (4). Four cellshad center/surround receptive fields, broad-band spectralsensitivities, and spherical dendritic arbors. These two celltypes will be considered in detail in a later paper.The magnocellular neurons (17 units) had large, radially

symmetrical dendritic fields with an average diameter of 300,uM (9, 18-21). Their dendrites often reached across the fullwidth of a layer; sometimes they extended into an adjacentinterlaminar zone and even into the next lamina. In spite oftheir occasional translaminar dendritic spread, these cellswere always driven by only one eye. They gave phasicdischarges to flashes of long duration, had center/surroundreceptive fields with relatively large centers (8'-2°), and werebroad-band in their responses to various colors (2).

Fig. 6 is a drawing of an on-center magnocellular neuronfound in layer 1. The cell's extensive dendritic field wasessentially circular and about 210 ,M in diameter. Somedendrites reached beyond the upper and lower borders of

5

1

FIG. 5. Reconstruction of an HRP-injected cell body found inparvocellular layer 5. This opponent color neuron was red on-center,green-off surround. It was influenced by the ipsilateral eye, and its3' field center was 40' from the center of the fovea. The basicallybipolar dendritic field was about 80 ,AM wide and was orientednormal to the borders ofthe layer. Small and large red spots producedsustained on responses, whereas annuli and large spots ofgreen lightinhibited the cell and elicited off discharges. Scale, 100 uM.

FIG. 6. Drawing of a magnocellular neuron injected in layer 1.The spherical dendritic field was =210 ,uM across. Some dendritesreached out of the lamina, but the cell was driven only by thecontralateral eye. The cell gave transient on responses to smallcentered white spots, but diffuse light (white or color) was withouteffect, indicating that the antagonistic surround was very strong. Thefield center of this broad-band neuron was 20' in diameter and was30 from the fovea. Scale, 100 ,uM.

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Proc. Natl. Acad. Sci. USA 85 (1988)

layer 1. The beaded structure of the dendrites was similar tothat of the parvocellular neurons, except that the beads of themagnocellular neuron were generally larger. The cell wasdriven only by the contralateral eye. Small white spotsrevealed that the cell's field center was 20' in diameter; it hada very strong antagonistic surround. This cell did not respondto diffuse colored stimuli and in all ways tested failed to showany evidence of opponent-color organization. Its area-re-sponse curves resembled those in Fig. 4.

DISCUSSIONThe results reported here provide additional informationabout the structural basis for the segregation of function inthe LGN of the monkey. In support of previous physiological(3-5, 15, 22) and anatomical studies (13, 14, 23, 24), thepresent findings demonstrate that the color-coded ganglioncells in the retina project exclusively to the parvocellulargeniculate layers, whereas the broad-band cells send theiraxons to the magnocellular laminae. In addition to theirspecific destinations, these two classes of optic-tract fibershave structurally distinct arborizations. Studies from thislaboratory (6, 7), as well as elsewhere (8), have also revealeddifferent terminal patterns for the X and Y optic-tract fiberssynapsing in the LGN of the cat. The X axons have narrowcolumnar terminations similar to those of the optic-tractfibers ending in the parvocellular layers of the monkey. TheY fibers in the cat have two types of arborizations, dependingupon their field-center sign. The on-center axons have arborsshaped like hour glasses, whereas the terminals of the off-center fibers have the appearance oftruncated cones. Neithertype of Y fiber has spherical arborizations, which are typicalof the axons ending in the magnocellular layers of themonkey.There is clear segregation of the retinal afferents going to

the parvocellular layers. On-center fibers project almostexclusively to laminae 6 and 5, whereas the axons ending inlayers 4 and 3 are nearly all off-center units. Schiller andMalpeli (4) first noticed this dramatic separation, using bothsingle-unit and multiple-unit extracellular recordings. Otherextracellular studies (2, 16) have reported only a partialsegregation of the two geniculate cell types, with on-centerneurons dominating in layers 6 and 5 and an even balance ofon- and off-center units in laminae 4 and 3.The HRP-injected cell bodies in the LGN of the monkey

are as structurally distinct as their retinal afferent inputs. Thered/green opponent-color cells in the parvocellular layershave bipolar dendritic fields. The X cells in the LGN of thecat have a very similar structure (9). The broad-band cells inthe magnocellular layers of the monkey, as well as the Y cellsin the LGN of the cat (9), have large, spherical dendriticarbors that sometimes extend into an adjacent lamina. Golgistudies of the LGN of the monkey have revealed a variety ofcell types, including the two major classes seen in this study(2, 9, 14, 21). There is some disagreement in the literatureabout the laminar distribution of the different cell classes.Nevertheless, the consensus seems to be that bipolar genic-ulate cells are more common in the parvocellular layers,whereas neurons with spherical, translaminar dendritic fieldsare more prevalent in the magnocellular laminae.

Within a given physiological class there is a close corre-spondence between the terminal patterns of the optic-tractfibers and the dendritic fields of the geniculate cells uponwhich these axons are presumably making synaptic contact.Conley et al. (12) have recently reported similar results in ananatomical study of the optic-tract fibers terminating in thelateral geniculate nuclei of Galago and Tupaia. In the cat (6-9) the arborizations of the X optic-tract fibers match the

dendritic shape of the X geniculate cells; both have a narrowcolumnar orientation perpendicular to the laminar bound-aries. What functional significance these structural relation-ships have for neural integration in the LGN remains to beshown.

Earlier studies of the LGN in the cat revealed that singleY optic-tract fibers from the contralateral eye terminated inboth layer A and layer C, whereas individual Y fibers fromthe ipsilateral eye ended in A1 and occasionally also in C1; Xaxons always arborized in a single geniculate layer (6-8).Given these results one might have expected that a pair ofparvocellular laminae associated with a given eye wouldshare common inputs from single optic-tract fibers. Instead,individual axons always synapsed in only one geniculatelayer, just as Conley et al. (12) found to be the case in Galagoand Tupaia lateral geniculate nuclei. Consequently, an ocularpair of parvocellular layers (e.g., layers 6 and 4) receivedseparate retinal afferents, even though both laminae got inputexclusively from the contralateral eye. This result is notentirely surprising because the members of an eye-relatedpair appear to be performing opposite contrast-detection func-tions (on- versus off-center). In fact, the combination of eyeinput and receptive-field center sign leads to each of the fourparvocellular layers being functionally distinct.

I thank Douglas Bowling for his participation in the early exper-iments, Faye Gomes for carrying out the histological procedures, andIrving Diamond for his constructive criticism and support of themanuscript. This research was supported by National Eye InstituteGrant EY 00568.

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