dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial...

Dissociation of the MedialPrefrontal, Posterior Parietal, andPosterior Temporal Cortex forSpatial Navigation andRecognition Memory in the Rat

Bryan Kolb, Kristin Buhrmann, Robert McDonald,and Robert J. Sutherland

University of Lethbridge, Lethbridge, Alberta, CanadaT1K 3M4

Rats with lesions of the medial prefrontal, posterior pa-rietal, or posterior temporal cortex were tested in fivespatial navigation tasks, which varied in egocentric orallocentric demands, a visual discrimination task, andtwo delayed nonmatching-to-sample tasks. Rats withprefrontal lesions were impaired at every spatial nav-igation task, whereas rats with posterior parietal le-sions had selective spatial navigation impairments.Rats with prefrontal lesions were also impaired at avisual delayed nonmatching-to-sample task, as theywere unable to learn the task, even with no delay. Theresults are consistent with the idea that the basic planof mammalian cortex includes prefrontal, posterior pa-rietal, and posterior temporal regions, each of whichhave generally similar functions across mammaliantaxa. There are, however, species-typical differencesthat reflect specific ecological pressures on the devel-opment of the different regions.

Although mammalian neocortex is remarkably similarin general structure across species (e.g., Kaas, 1987;Rockel et al., 1980), there are significant species dif-ferences both in the details and in the complexity ofits organization For example, although there are mul-tiple representations of the sensory inputs to the cor-tex of all mammals, the number of cortical regionswithin a single modality, as well as the details of theirconnectivity and functions, appear to differ in evenrelatively closely related species such as Old and NewWorld monkeys (e.g., Kaas, 1987). Nonetheless, theneocortex is presumably based upon a general planof organization that was present in ancestors commonto living mammals. Furthermore, if this general planwere understood, it would provide some insight intothe organization of brains of larger-brained animalssuch as humans. Thus, the chief purpose of many ofour studies over the past 20 years has been to under-stand the general organization of cortical function(e.g., Kolb et al., 1974, 1983; Kolb, 1984, 1990a).

An intriguing aspect of cortical organization in pri-mates is that the prefrontal, posterior parietal, and in-ferotemporal cortex are proposed to be involved inthe control of "higher cognitive functions." Thus, dam-age to these regions produces a variety of cognitivedisturbances in humans in the absence of primary sen-sory or motor loss (e.g., Kolb and Whishaw, 1990).Theprincipal purpose of the present studies was to com-pare the relative contributions of the putative analogsof the prefrontal, posterior parietal, and posterior tem-poral cortex in rats to the control of spatial navigationand recognition memory.

A primary concern in studies of this type is to de-termine that the tissue involved in different species is"equivalent." The traditional way is to search for ho-mologies. Since brains leave poor fossil records, thismust be done indirectly. Campbell and Hodos (1970)proposed that similarities in several criteria could beused. We have focused upon two of these: connectiv-ity and behavioral changes from lesions Thus, in thepresent study the regions were chosen on the basisof connectivity (Fig. 1). Zilles's (1985) areas Cgl, Cg3,IL, and part of Fr2 were removed in the prefrontal(PFQ group. This cortex receives projections from thedorsal medial region (MD) of the thalamus (Groene-wegen, 1988), as well as corticocortical connectionsfrom occipital cortex, somatosensory cortex, posteriorparietal cortex, and posterior temporal cortex (Kolb,

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Oc2Ml

Figure 1. Comparison of Kneg's (1946) and Zilles's (1385) cytoarchitectonic divisions of the rat's cerebral cortex.

1990b; Uylings and van Eden, 1990). The posteriortemporal cortex was identified as Zilles's Te2 and Te3.This region may receive thalamic projections from thelateral posterior (LP) nucleus (for a review of the ev-idence, see Dean, 1990). It also appears to receive vi-sual cortical projections from Ocl and Oc2L (Dean,1990) and is connected with the contralateral hemi-sphere via the anterior commissure (Horel and Stelz-ner, 1981; B. Kolb, unpublished observations). Finally,it sends a small projection to prefrontal region IL(Kolb, 1990b). Defining the posterior parietal regionis more problematic. Krieg (1946) identified a regionbetween visual and somatosensory cortex that hecalled area 7 (Fig. 1). This region is part of Zilles'sOc2M since, unlike the prefrontal and temporalregions, it is not easily distinguished on cytoarchitec-tonic grounds. Nonetheless, this region receives and

sends connections to the prefrontal cortex as well asdifferent parts of the occipital and somatosensory cor-tex (Kolb and Walkey, 1987; Reep et al., 1987; Kolb,1990c; Chandler et al., 1992). Although Kesner and hiscolleagues have included tissue well beyond theboundaries of the LP and prefrontal connections toinclude part of Zilles's Parl, Oc2L, and Tel (e.g., Di-Mattia and Kesner, 1988a,b; Kesner et al., 1991), wechose to restrict our lesions to the region that, onanatomical grounds, appears to be most similar to theposterior parietal cortex of primates (Fig. 1).

Rats were given lesions of the prefrontal, posteriortemporal, or posterior parietal cortex and were sub-sequently tested on five spatial navigation tasks, whichvaried in the allocentric or egocentric demands, a vi-sual discrimination task, and two delayed nonmatch-ing-to-sample tasks (see Table 1).

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Table 1Summary of groups trained

Task

MomsAggleton DNMSLandmarkVisual discriminationLandmarkMorris (pretramed)Egocentric radialMumby DNMS

on each task

Experi-ment

11112345

Group

CON

XXXXXXXX

PFC

XXXXXXXX

PPC

XXXXX

X

PTC

XXXX

X

X indicates that animals in this group were tested in the task. CON, normalcontrol group; DNMS, delayed nonmatching to sample; PFC, prefrontal cortexgroup; PPC, posterior parietal cortex group; PTC, posterior temporal cortexgroup.

Five sets of experimental animals were used in thisstudy. Since different sets of animals were treated dif-ferently, the procedures for each set of animals aredescribed separately. The results are described in a sin-gle section, however, to simplify explanation.

Materials and Methods

Experiment 1In this experiment rats with lesions of the prefrontal,posterior parietal, or posterior temporal cortex weretrained in the Morris water task (Morris, 1981), theAggleton visual nonmatch-to-sample task (Aggleton,1985), the "landmark" water task (Kolb and Walkey,1987), and a visual discrimination task.

SubjectsThe studies were done with 28 male rats, derived fromCharles River Long-Evans strains, which were dividedinto four groups of seven rats: (1) normal control(CON), (2) medial prefrontal cortex lesion (PFC), (3)posterior parietal cortex lesion (PPC), and (4) poste-rior temporal cortex lesion (PTC). The animals werehoused individually in stainless steel hanging cagesand maintained on ad libitum water and 12:12 hrlight/dark schedule throughout the experiments. Theanimals were on ad lib food throughout, with the ex-ception of the time spent in the nonmatch-to-sampletasks, when they were maintained at 90% ad libweight.

Surgical ProceduresThe animals were anesthetized with sodium pento-barbital (60 mg/kg). The frontal neocortex was ex-posed by first making a small burr hole along the pa-rietal suture and then removing the skull withrongeurs from the bregmoidal junction anteriorly 5mm and laterally 3 mm on each side of the midline.The posterior parietal cortex was exposed by remov-ing the skull from 3 to 6 mm posterior to the bregma,and lateral 1.5 mm from the sagittal suture to the tem-poral crest, which is about 4 mm lateral. The temporalcortex was exposed by cutting the temporal muscle

at the temporal crest and then retracting it to allowaccess to the temporal region. A small hole wasopened with a drill from -5.5 to -8.5 mm relative tobregma, beginning about 2 mm below the temporalcrest. The skull removal was enlarged to the rhinalfissure with fine tipped rongeurs. For each removalthe dura and underlying gray matter were cut alongthe edge of the skull opening with a #11 scalpel blade.The exposed neocortex was removed by aspirationwith the aid of a surgical microscope. The externalcapsule was left in place to reduce the chance of in-advertently damaging the underlying tissue. Followinghemostasis the scalp wound was closed with woundclips. The controls were anesthetized, the skin incised,and clipped closed.

Anatomical ProceduresAfter all behavioral testing was complete the rats weregiven an overdose of sodium pentobarbital and intra-cardially perfused with 0.9% saline followed by 10%formalin in saline. The brains were removed, weighed,and placed in 30% sucrose formalin for about 1 week.They were photographed and then cut frozen at 40(i.m. Every 10th section was saved and mounted onslides for later cresyl violet staining.

Morris Water TaskThe method followed in this test is virtually identicalto that used by Sutherland et al. (1983). The mazeconsisted of a circular pool (1.5 m diameter, 45 cmheight), the inside of which was painted white andfilled to a height of 25 cm with approximately 18°Cwater in which enough instant powdered skim milkwas dissolved to render the water opaque. A clearPlexiglas platform (11 X 12 cm) was present insidethe pool; its top surface was 1 cm below the surfaceof the water, and thus the platform was invisible to aviewer inside the pool (Fig. 2).

A trial consisted of placing a rat by hand into thewater, facing the wall of the pool, at one of the fourstarting locations (north, south, east, or west), aroundthe pool's perimeter. Within each block of four trials,each rat started at the four starting locations, but se-quence of locations was randomly selected.

The behavioral testing was conducted on 5 consec-utive days, with each rat receiving eight trials per day.If on a particular trial a rat found the platform, it waspermitted to remain on the platform for 10 sec. A trialwas terminated if a rat failed to find the platform after90 sec. At the end of a trial, the rat was returned to aholding cage, and approximately 5 min elapsed beforebeginning the next trial. The swimming path for eachtrial was recorded via a video camera mounted abovethe tank A computer system was able to extract theblack head of the rat from the white background ofthe milk and then subsequently to determine the an-gle relative to the platform that the rat was heading12 cm (approximately one body length) after release(heading error). The latency to find the platform (es-cape latency) was timed by an experimenter standingby the pool's edge Testing began 4 weeks after thesurgery.

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Mumby DNMS

Morrl» Water Task Landmark Water Task

•" o„ ^ o

Aggleton DNMS

Egocentric Radial Arm Maze

T1

T1

T2

T 8

Figure 1 Schematic illustrations of the mazes used in the present study. 6, goal; S, start location; I trial

Aggleton Nonmatching-to-Sample TaskThe method used in this test is similar to the methodfirst described by Aggleton (1985). The rats were test-ed in a Y-maze in which the start box and two goalboxes were removable (Fig. 2). In each trial the startbox matched one of the goal boxes and differed fromthe other. The rats' task was to select the goal box thatdiffered from the start box (nonmatch to sample). Thegoal boxes were changed on every trial.

Each arm of the wooden Y-maze was 13 cm wideX 20 cm high X 20 cm long. Twenty pairs of hard-board boxes served as start and goal boxes. Theseboxes were fitted into the end of each arm, making atotal length of 26 cm. Each pair of boxes was distinctfrom every other pair in that the walls and floor werepainted in a distinctive pattern using white, gray, and/or black paint. If an animal chose the correct box, itwas allowed to lick chocolate chip slurry from a spat-ula held at the end of the alley by the experimenter.The spatula was not presented to the animal until itran to the end of the goal box.

The animals were habituated to the Y-maze for 3 d.They were then trained for 2 d to run down the alleysto get mash from the spatula. The experiment thenbegan. To start each session the animal was placed inan arm for 20 sec, after which the door was removed

and the animal was allowed to choose between twoarms, each of which contained a different goal box,one of which was identical to the start box. The ratwas considered to have chosen when all four pawsentered an arm. If the animal's choice was correct, itwas fed and then the animal was held in the alley for20 sec while the new pairs of boxes were placed inthe arm. If the animal's choice was incorrect, it wasplaced in the correct arm and held for 20 sec. Thedoor was then raised and, once again, the animal wasallowed to choose (Fig. 2). The animals were trainedfor 10 trials per day to a criterion of 5 consecutivedays at 80% correct. After reaching criterion on thenonmatch-to-sample portion of the test, the animalsbegan delay training. The procedure was identical tothe nonmatch to sample, except that after 20 sec inthe start box the animals were released into the cen-tral section of the maze (Fig. 2) and held there for 10sec. Once they reached criterion at 10 sec, they wereshifted to a 20 sec delay. They were trained to crite-rion or for 10 d (200 trials), whichever came first.

Landmark TaskThe method followed in this test was identical to thatused by Kolb and Walkey (1987). The same watermaze was used as in the Morris task but there was

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one essential difference to the procedure: the plat-form moved on each block of trials and its locationwas marked by a "landmark," which was an 18.5 cmX 14 cm black rectangle mounted on the maze wallapproximately 25 cm away from the platform (Fig. 2).There were only three trials per block, each of whichbegan from one of the locations indicated in Figure 2.Thus, there were only six trials per day. The behavioraltraining was carried out as in the Morris task but onlythe escape latency was recorded. Testing began afterall animals had completed the Aggleton Ymaze, whichwas about 6 weeks after the Morris maze testing.

Visual Discrimination TaskThe same water tank was used as in the other watertasks The platform had a 5-cm-diameter ball, attachedto the platform such that it appeared to sit on thesurface of the water. A second ball was attached to athin pole but there was no escape platform. The ballswere painted in alternating 1-cm-wide black andwhite stripes with the stripes on the platform ball ori-ented vertically and those on the pole ball orientedhorizontally. The platforms were located approximate-ly 30 cm from the wall and 50 cm apart (Fig. 2). Inthis task the rats always began from the same startlocation and were to swim to the platform, the loca-tion of which was marked by the vertical striped ball.If an animal swam to the wrong location it was al-lowed to self-correct. The location of the stimuli var-ied according to a Gellerman series. The experimenterrecorded the latency to escape to the platform as wellas whether or not the correct location was initiallyselected. The animals were given eight trials per dayfor 5 d.

Experiment 2Since the rats in experiment 1 learned two spatial nav-igation tasks in the same water tank, it was possiblethat the prior testing in the Morris task had affectedperformance in the landmark task in experiment 1.Therefore, in this experiment the animals were trainedonly in the landmark task. Only control rats and ratswith prefrontal or parietal lesions were included.

Subjects and ProceduresThe studies were done with 24 female rats, derivedfrom Charles River Long-Evans strains, which were di-vided into three groups of eight rats: (1) normal con-trol, (2) medial prefrontal cortex lesions, and (3) pos-terior parietal cortex lesion. The animals were housedindividually in stainless steel hanging cages and main-tained on ad libitum food and water and 12:12 hrlight/dark schedule throughout the experiments. Theprocedures were generally similar to those in experi-ment 1, the lone exception being the anesthetic dose,which was reduced to 45 mg/kg for female rats.

Experiment 3When the rats with frontal lesions are trained in theMorris water task they are impaired at finding the plat-form. It is not clear, however, whether the deficit isone of learning the spatial location or learning the

strategies necessary to learn the location. To test thiswe pretrained rats to swim to a visible platform thatwas either in a fixed location or moved on every trial.They were then trained in the standard Morris task.Only control rats and rats with prefrontal lesions wereincluded.

SubjectsThe experiment utilized 30 male hooded rats, de-rived from Charles River breeding stock. The animalswere divided into six groups: (1) normal control withno pretraining (n = 4), (2) frontal with no pretrain-ing (n = 6), (3) normal control with pretraining tothe fixed location (n = 4), (4) frontal with pretrain-ing to the fixed location (n = 6), (5) normal controlwith pretraining to the moving location (n = 4), and(6) frontal with pretraining to the moving location(n = 6). Surgical procedures and housing were as inexperiment 1.

Testing ProceduresThe rats in the pretraining groups were given fourtrials per day for 4 d in the same tank as was used inexperiments 1 and 2. The general procedure was iden-tical to the Morris task procedure used in the earlierexperiments, except that a 15 X 15 cm platform,which was painted black and extended 1 cm abovethe water level, was either located in a fixed locationin the tank or moved randomly from trial to trialaround the tank, such that it was never in the samelocation on two trials on one test day. The rats withoutpretraining were left in their cages during this phaseof testing. Three days after the completion of the pre-training, all of the rats were trained in the same tankusing the general Morris task procedure used in ex-periment 1. The hidden platform was located in thesame position as the fixed visible platform had beenplaced in pretraining. Animals were trained for fourtrials per day for 6 d and the latency to find the plat-form was recorded. On the last two test days the an-imals' swim patterns were drawn manually by an ob-server seated near the edge of the pool.

Experiment 4The rats in this experiment learned a novel version ofthe radial arm maze. The animals were placed at thedistal end of an arm and had to learn to run to theadjacent arm to the right. Only control rats and ratswith prefrontal or parietal lesions were included.

SubjectsThe studies were done with 18 male rats, derived fromCharles River Long-Evans strains, which were dividedinto three groups of six rats. (1) normal control, (2)medial prefrontal cortex lesion, and (3) posterior pa-rietal cortex lesion. The animals were housed individ-ual!)' in stainless steel hanging cages and maintainedon ad libitum water and 12:12 hr light/dark schedulethroughout the experiments. The animals were main-tained at 90% ad lib body weight.

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ProcedureThe symmetrical eight-arm maze featured 60 cm armsprojecting from a center circular platform (38 cm),each arm having a width of 9 cm and bordered by 2.5cm walls on either side (Fig. 2). A recessed food traywas located at the end of each arm. The assembly wasmounted 95 cm above the floor in a small room whereall distal visual cues were kept constant.

Animals were adapted to the male for 2 d by plac-ing them in the center platform in pairs and then al-lowing them to search for chocolate chip cookiemash, which was placed in the food trays. This wasthen repeated for 2 additional days as the animalswere tested individually. Testing began on the fifth day.Animals were placed by hand onto the end of an arm,facing the center platform, and allowed to search forchocolate-chip cookie mash placed only in the traylocated in the adjacent alley to the right (Fig. 2). Oncethe animals had made a choice and had run to theend of an alley, they were allowed to eat the food (ifcorrect) and then were removed from the maze forapproximately 5 min. They were given eight trials perday, each of which began from a different arm. Theorder of starting arms was according to the pseudo-random schedule. Animals were tested to a criterionof seven of eight correct. An arm entry was registeredif the rat placed all four of its feet within the alley. Atthe completion of testing, the animals were sacrificedand the brains processed as in the previous experi-ments.

Experiment 5Rats were trained in a delayed nonmatching-to-sampletest devised by Mumby (Mumby et al., 1989). Onlycontrol rats and rats with prefrontal or temporal le-sions were trained in this task

SubjectsThe studies were done with 18 male rats, derived fromCharles River Long-Evans strains, which were dividedinto three groups: (1) normal control (n = 8), (2) me-dial prefrontal cortex lesion (n = 5), and (3) posteriortemporal cortex lesion (n = 5). One of the rats witha medial frontal lesion became ill partway through theexperiment and did not complete testing. His datawere not included in the analyses. The animals werehoused individually in stainless steel hanging cagesand maintained on ad libitum water and 12:12 hrlight/dark schedule throughout the experiments. Theanimals were maintained at 90% ad lib body weight.

ProcedureRats were tested in a wooden shuttle box, which wasdivided into three equal-sized sections, each measur-ing 20 cm wide X 20 cm long (Fig. 2). There was alid to the center section and the entire maze waspainted light gray. The animals first were habituatedto the maze for 2 d, during which they learned to findFroot Loops in the 2-cm-diameter recessed food wells(Fig. 2). When training began the animals were placedin the central start box and allowed to displace anobject that covered one of the food cups. The animals

figure 3. Surface reconstructions of typical lesions in each group.

received one-half of a Froot Loop, which they usuallytook back to the start box to consume. The other startbox door was then raised and the animals were al-lowed access to two different objects, one of whichwas the same as the displaced object. The rats' taskwas to displace the novel object to receive reward.There were 40 pairs of junk objects, which varied insize, color, and texture. They were made of metal, plas-tic, rubber, glass, or painted wood, and included suchthings as ping pong balls, rubber erasers, empty softdrink cans, and so on. If the animal was correct it wasgiven the food reward and it returned to the start box.If it was incorrect, it was returned to the start box bythe experimenter. Approximately 30 sec later the nexttrial began. Animals were trained for 15 trials per dayto a criterion of 2 consecutive days of 80% correct, orfor 500 trials, whichever came first. After the animalsreached criterion at the nonmatching task, a delay wasintroduced. Thus, after the animals had retrieved thereward under the sample object, they were locked inthe start box for 10 sec before being allowed accessto the pair. Once the animals reached criterion at 10sec, they were trained on a delay of 20 sec.

Results

Anatomical ResultsThe lesions in each experiment were comparable andremoved the tissue as intended. Thus, the prefrontallesions removed all of Cg3, the anterior portion ofCgl, variable amounts of IL, the medial part of Fr2,and occasionally part of MO (Figs. 3, 4). There wassubtle retrograde degeneration in the posterior lateralpart of MD and the anterior medial thalamus. The le-sions did not invade the striatum, nor did they includethe taenia tectae or olfactory structures. The posteriorparietal lesions were restricted to dorsal cortex, re-moving the anterior portion of Zilles's Oc2L andOc2M and in some cases the most anterior portion ofOcl (Fig. 4). There was no damage to either the retro-splenial cortex or the underlying hippocampal for-mation. There was retrograde degeneration through-


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PFC PPC TE2/3

figure 4. Serial reconstructions of the lesions from each brain illustrated in Figure 3.

out the lateral posterior nucleus and portions of thelateral dorsal nucleus. The temporal lesions includedmost of areas Te2 and Te3, and variable amounts ofthe posterior portion of Tel and the lateral portion ofOc2L. In addition, most lesions included the perirhinalcortex below Te2/3 and in some cases there wasslight unilateral damage to entorhinal cortex. Therewas no damage to the underlying hippocampal for-mation. There was retrograde degeneration in the lat-eral posterior nucleus as well as the medial geniculatenucleus.

To estimate the loss of brain tissue following thedifferent lesions, we weighed the brains immediatelyafter removal in experiment 1. The pineal gland andparaflocculi were removed, the spinal cord wasblocked even with the back of the cerebellum, andthe olfactory bulbs were blocked at the level of theanterior tip of the frontal pole. Total loss of brainweight in each of the lesion groups was rather small,measuring less than 10% of total brain weight (Table2), with no real difference between any of the lesiongroups. ANOVA showed a significant effect of group[flC3,24) = lO.86,p < 0.001]. Follow-up tests (Fisher's

Table 2Summary of brain weights

Group

ControlPrefrontalPosterior parietalPosterior temporal

in experiment 1

Weight |gm)

2.248 ± 0251091 ± 0.020Z097 ± 0.0292.080 ± 0.025

% Control

100939392

Numbers indicate means and SEs.

LSD, ps < 0.01) indicated that each of the lesiongroups differed from the control group but not amongthemselves. Thus, it appears that differences in the be-havioral effects of the lesions among the groups donot result from differences in lesion size.

Behavioral Results

Morris Water TaskWhen initially placed in the tank, normal control ratstraverse a wide area, zigzagging across the tank untilthey bump into the hidden platform. Then they climbonto the platform and rear up a number of times. Per-formance of these rats improves rapidly on successivetrials, and within three trial blocks of the rats havereached asymptote, locating the platform within about6 sec from any start location (Fig. 5). The rats withtemporal lesions were virtually identical to the con-trols, as they learned the task quickly and were asaccurate in swimming to the platform as the controlanimals. The rats with parietal lesions were impairedat the task, and were never as accurate as controls inswimming to it. Thus, their final swim latencies wereconsistently 3-4 sec slower than control or temporallesion rats. The rats with prefrontal lesions were theslowest to learn the task, and like the parietal rats, stillwere not accurate in swimming to the platform at theend of training. Thus, whereas the control and tem-poral animals had final heading angles (see Fig. 5)around 19°, the parietal and prefrontal groups werestill around chance, which is about 40°. Two measureswere analyzed statistically: (1) latency to find the plat-form, and (2) the angle at which the rat swam relativeto the platform. (Owing to a computer malfunction,

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A. Morris Water Task: Latency A. PRETRAINING

OCNPFCPPCPTC

-r

TEf

5LU

a.

ALE

SO

i—

70

60

50

40

30

20

10

0

Trial Block

B. Morris Water Task: Heading Error80-I

$ 7 0 -

2

6 0 -

5 0 -

<0 -

3 0 -

2 0 -

10

OCNPFCPPCPTC

Trial Block

C. Morris Water Task: Total Latency

PTC

figure 5. Summary of Morris water task performance A Latency to find theplatform for each group on each tnal block. B, Swim heading error, which isexpressed in degrees, over each trial block. Chance performance is approx-imately 39°. Rats with prefrontal or parietal lesions were at chance perfor-mance at the end of training. C, Total escape latency summed over the 10trial blocks. Rats with prefrontal lesions were also impaired, especially atheading error. CON, control; PFC, prefrontal cortex; PPC, posterior parietalcortex; PTC, posterior temporal cortex.

the heading angles were not available for trial blocks3 and 4.)

ANOVA on the escape latency (group X trial block)revealed a significant main effect of group [,F(3,24) =92, p < 0.001], trial block [f(9,215) = 40.1, p <0.001], and the interaction [^27,215) = 7.2, p <0.001]. Fisher's LSD (ps < 0.05 or better) showed thatthe control and temporal groups differed from boththe parietal and prefrontal groups. The prefrontalgroup was significantly poorer at the task than theparietal group.

ANOVA on the heading angles also revealed signifi-cant main effects of groups [^3,24) = 6.7,p = 0.002]and trial block [/=(7,l65) = 15.4,p < 0.001], but theinteraction was not significant [F(21,165) = 1.2, p =0.27]. Post hoc comparisons of the heading angles on

DD HXH>

CONTROL FRONTAL

B. TEST PHASE

5LU

%

LU

• FOE• IO/NQ• HXH5

CONTROL FRONTAL

C. ERRORS ON TEST PHASE

• K>ED MDVW3• RXH>

CONTROL FRONTAL

Figure 6. Summary of Morns task performance for the rats given pretrainingto a visible platform. A, Pretraining latency scores over four training blocks.B, Total latency scores over six trial blocks in the test phase, which was onthe standard Morns task. C, Errors on the last day of training in the testphase. NONE, no pretraining experience; MOVING, pretraining to a movingvisible platform, FIXED, pretraining to a stationary visible platform

trial block 10 showed the control and temporalgroups to differ from the other two groups, which didnot differ between themselves.

Morris Water Task: Pretraining ExperienceBoth the control and frontal rats learned to find thevisible platform rapidly in the pretraining phase, re-gardless of whether it was in a fixed or variable lo-cation (Fig. 6). This result suggests that the deficit ob-served in the Morris task by frontal animals is not aproblem with swimming but is due to some aspect ofthe task requirements. When the pretrained animalswere shifted to the hidden platform condition, therewere two clear results. First, pretraining control ratsto swim to a. fixed visible platform was clearly bene-ficial. They not only learned that there was an escapeplatform but also appeared to learn its location. Incontrast, pretraining control rats to a moving visibleplatfonn had only a small effect upon later perfor-mance in the Morris task. Second, pretraining rats with


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A. Landmark Task: Exp 1

> 3 5 O 1^ 300-

5 250

LU 200-

150

100-

OCN PFC PPC PTC

B. Landmark Task: Exp 2

IOCN PFC PPC

C. Landmark Task: Exp 2

40-

20-

CTN

PPC

PPC

2 1 2 3 4 5 B 7 8 S 1 0TRIAL BLOCK

Figure 7. A and B, Summary of landmark water task performance in eachexperiment Data represent total escape latency summed over the 10 trialblocks. Rats with prefrontal lesions were the most impaired group in eachexperiment C, Latency to find the platform on each trial block in the secondlandmark task expenment CON, control; PFC, prefrontal cortex; PPC, poftenorparietal cortex; PTC, posterior temporal cortex.

frontal lesions to swim to a visible platform was alsobeneficial but it made no difference whether the plat-form was fixed or moving. That is, the frontal rats ap-peared to learn that there was an escape platform anda strategy to swim to it but they did not learn its lo-cation. We analyzed two performance measures: es-cape latency and errors.

Escape latency. ANOVA on the pretraining escapelatencies showed that there was neither a lesion effect1/^1,15) = 2.1,/> = 0.17], a condition (fixed vs mov-ing) effect [/^1,15) = 0.70, p = 0.42 nor an interac-tion [/=C1,15) = 1.1, p = 0.32], However, ANOVA onescape latency in the second phase of training (theMorris task) showed significant effects of lesion[7^1,23) = 28.5, p < 0.0001], condition [/=(2,23) =25.5,p < 0.0001], and the interaction [/=(2,23) = 9.6,p < 0.0009]. Post hoc tests (Fisher's LSD.ps < 0.05)confirmed what is visible in Figure 5. Thus, these anal-yses showed that (1) control rats that were trained tothe fixed visible platform performed significantly bet-

ter than the other control groups, (2) pretraining sig-nificantly improved the performance of both groupsof pretrained frontal rats, and (3) the control rats pre-trained on a fixed platform performed better than anyother group.

Errors. The error measure gives an estimate of theaccuracy of spatial navigation. Thus, if the rat swimsdirectly to the platform via an imaginary corridorabout 20 cm wide, it is scored as correct. In contrast,if it deviates from the corridor, it is scored as incorrect.On any given day an animal could therefore make asmany as four errors (i.e., one per trial). Examinationof the error scores of the control animals shows thaton the last day of training those in the pretraininggroups performed rather well, making only one error.The naive control animals made more than twice asmany errors, reflecting their poorer performance.Nonetheless, even the naive control animals were cor-rect on half of the trials, indicating that they hadlearned the approximate location of the platform. Incontrast, the rats with frontal lesions performed poor-ly. The naive frontal animals averaged nearly four er-rors and the pretrained frontal rats averaged nearlythree errors. Hence, the frontal animals did not appearto have learned the location of the platform. Indeed,direct examination of the swim paths confirmed thisconclusion as the frontal animals had learned to swimparallel to the pool wall and about 20 cm away fromit, thus ensuring that they would bump into it. ANOVAon the error scores revealed a main effect of lesiongroup [/(1,23) = 38.1, p < 0.0001] and condition[f(2,23) = 32, p = 0.06] but not the interaction[/=(1,23) = 0.5,p = 0.6]. Post hoc tests dps < 0.05)indicated that the frontal groups differed from theirrespective control groups in each condition.

Landmark Task: Experiment 1Control rats learned to swim to the platform veryquickly, presumably because they were familiar withthe general problem of locating a platform in the wa-ter. In the first trial block the animals tended to swimin the region that the platform had been located inthe Morris task but they quickly abandoned this lo-cation and began to search the pool. The animalsquickly learned the new task, however, and were ableto swim relatively directly to the platform by the fifthtrial block (Fig. 7). The rats with temporal lesions werea bit slower in acquiring the task but by the fifth trialblock they too were at asymptote. The rats with pa-rietal or prefrontal lesions were much slower to ac-quire the task and neither group ever learned to swimdirectly to the platform. As we have described in detailelsewhere (see Kolb and Walkey, 1987, their Fig. 9),they learned to swim a circular route about 10 cmfrom the tank wall, which allowed them to bump intothe platform.

ANOVA on the escape latency failed to show a maineffect of group [F(23,24) = 2.38,p = 0.09], but therewas a main effect of trial block (fl[9,2l6) = 6.5,p <0.001]. The interaction was not significant [F(27,2\6)= 1.3,/> = 0.15]. In view of the fact that there wasno overlap between the total latency scores of the

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control and parietal rats, we took the advice of Saville(1990) and proceeded with post hoc tests on the maineffect of group. Fisher's LSD (ps < 0.05) showed thatthe parietal rats differed from the control group butno other comparisons reached significance. The statis-tical results reflect, in part, the high variability of theperformance of the rats with prefrontal lesions. Sincewe had not expected the prefrontal animals to havedifficulties, we felt it best to replicate this test in ex-periment 2.

Landmark Task: Experiment 2The control animals acquired this task more slowlythan in experiment 1, presumably because they hadno previous experience in a water maze task. None-theless, they reached asymptote in about six trialblocks and by the end of training they were able toswim directly to the platform. Both of the lesiongroups were impaired, and the prefrontal group neverbecame particularly proficient. Analysis of swim pat-terns showed that in contrast to the control animals,neither the parietal nor prefrontal rats swim directlyto the platform but rather swam parallel to the tankwall until they struck the platform

ANOVA on the escape latencies showed a main ef-fect of group [7^2,21) = 3.9,p = 0.036], trial block[7^9,189) = 40.3, p < 0.001], and the interaction[7=1(18,189) = \.T7,p = 0.03]. Follow-up tests (ps <0.05) on the group effect showed that the controlgroup differed from both the prefrontal and parietalgroups, which did not differ from one another.

Egocentric Radial Arm TaskWhen compared to more traditional radial arm mazetasks, this version proved to be a difficult task for an-imals to learn. Thus, normal animals took an averageof 15 d and nearly 100 errors to reach criterion (Fig.8), whereas in our experience normal animals learnthe traditional radial arm task in about 5 d and 20errors. The most common error of control animals inthe egocentric version was to skip an alley and toenter the second alley, rather than the first alley to theright. We had the impression that often rats were run-ning too quickly to negotiate the sharp (45°) rightturn and thus headed down the next alley. Indeed, theanimals did not appear to be solving the task visuallyas they seldom "looked down the chosen alley" beforerunning down it. It thus seems likely that the animalsprimarily used kinesthetic information, rather than vi-sual information to solve the maze. Rats with posteriorparietal lesions were virtually identical to control an-imals. In contrast, however, rats with prefrontal lesionswere very poor at the task and often just ran straightacross the center platform to enter an alley oppositethe start alley. In fact, only two of the six prefrontalrats reached criterion after 25 d of testing. Rather, theanimals perseverated badly and simply continued torun down the alley and across the maze.

ANOVA on the errors was significant [7^2,15) =4.37,p = 0.03]. Follow-up tests (ps < 0.05) showedthat the prefrontal group differed from both the con-trol and parietal groups. The latter groups did not dif-

A. Egocentric RAM: Errors

(Ai-c

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o

2

CON PFC PPC

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20-

B. Egocentric RAM: Days

OCN PPC PPCFigure 8. Summary of performance in the egocentric radial arm maze. A,Errors to criterion. B, Days to criterion. Rats with prefrontal lesions were theonly group impaired at acquisition of the task. CON, control; PFC, prefrontalcortex; PPC, posterior parietal cortex.

fer. ANOVA on the days to criterion was also signifi-cant [7=1(2,15) = 4.02,p = 0.04]. Once again, post hoctests showed only that the prefrontal group differedfrom the other two groups.

In view of the unexpectedly severe deficit in ac-quisition by the prefrontal rats, we subsequently re-moved the prefrontal cortex of the control animals,waited 2 weeks, and then retested the animals for 15d, or until they reached criterion, whichever camefirst. Of the six animals, four reached criterion with amean of 53 errors, which was poor retention but wassomewhat faster than the original learning (mean of82 errors). However, the other two rats did miserablyand after 16 d they had three of eight and zero ofeight correct, respectively. Indeed, the latter rat hadonly 6 of 128 correct in the 16 d. In sum, it appearsthat there is both an acquisition and a retention deficitin this task for rats with prefrontal lesions. In contrast,

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posterior parietal lesions have no apparent effectupon performance, although we did not test retentionin rats with such lesions.

Aggleton Delayed Nonmatching to SampleThe control, posterior parietal, and prefrontal groupsperformed very similarly in the nondelay portion ofthis task as each group made an average of about 50errors and took about 17 d to criterion (Fig. 9), whichis approximately how Aggleton's animals performed.In contrast, the rats with temporal lesions performedvery poorly and none reached criterion after 25 d. Inview of the poor performance by the temporal lesiongroup, we decided not to test this group in the delaycondition. The other three groups had little difficultywith the 10 sec delay but when the animals wereshifted to a 20 sec delay the prefrontal group fell tochance performance and only one of seven rats re-gained criterion after 10 d of training (Fig. 9). Onecurious observation is relevant here. By the time theanimals had learned the original task they were wellhabituated to the maze and seldom left much fecalmatter in the maze. However, during the 20 sec delaycomponent the rats with prefrontal lesions dramati-cally increased their defecations in the maze, suggest-ing that they found this segment stressful. Unfortu-nately, we did not quantify this observation.

ANOVA on the errors to criterion on the nondelayportion of the task was significant [F(3,24) = 51.1, p< 0.001]. Multiple comparisons (J> < 0.01) indicatedthat the temporal group differed from each of the oth-er groups, who did not differ among themselves. ANO-VA on the 20 sec delay condition revealed a significanteffect [/•(2.18) = 7l.6,p < 0.001], and follow-up tests(/> < 0.01) showed that the prefrontal group differedfrom the other two groups, which did not differ be-tween themselves. Thus, this test successfully dissoci-ated the performance of all three lesion groups: theparietal group was unimpaired, the prefrontal groupwas impaired only with a delay, and the temporalgroup was unable to learn the basic task.

Mumby Delayed Nonmatching to SampleThe animals were very easy to test in the box, whichseems well suited to rats because of the "safe" darkregion in the center (Fig. 2). They did not acquire thetask quickly, however, as they took about 350 trials toreach criterion. Nonetheless, all animals but one tem-poral animal solved the nonmatch-to-sample task, aswell as the 10 and 20 sec delayed conditions (Fig. 10)ANOVA on errors to criterion on the nonmatchingportion [7^2,16) = 1.33, p = 0.30], 10 sec delay[/=(2,15) = 0.42,p = 0.67], and 20 sec delay [7=1(2,15)= 0.86,p = 0.45] were all nonsignificant.

Visual Discrimination TaskControl animals learned this task rapidly and were per-forming near 80% correct by the second trial block.The rats with parietal lesions performed as well as thecontrol rats and the animals in the other two groupswere only slightly slower in learning the task (Fig. 11).There was one interesting difference between the

A. Aggleton nonmatch-to-sample

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figure 9. Summary of performance in the Aggleton nonmatching-to-sampletask. A, Total errors to criterion with no delay. Rats with posterior temporallesions failed to leam the task. B, Total errors to criterion on the 20 sec delaytest Rats with prefrontal lesions failed to learn the task. C, Percentage cor-rect in the different phases of the task for the control and prefrontal groups.CON, control; DNMS-W, delayed nonmatching to sample with 10 sec delay,DNMS-20, delayed nonmatching to sample with 20 sec delay; NMS, non-matching to sample with no delay; PFC, prefrontal cortex; PPC, posteriorparietal cortex; PTC, posterior temporal cortex.

groups, however; the rats with parietal lesions, and toa lesser extent prefrontal lesions, were slower to findthe platform.This did not appear to be due to a slowerswimming speed in these animals but rather becausethe animals did not take as direct a route to the cor-

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Figure 11. Summary of performance on the horizontal-vertical stripes dis-crimination. There was no significant difference among the groups in per-centage correct CON, control, PFC, prefrontal cortex; PPC, posterior parietalcortex; PTC, posterior temporal cortex.

B. Mumby delayed nonmatch-to-sample

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Figure 10. Summary of performance on the Mumby nonmatching-to-sampletask A, Errors to criterion in the initial acquisition of the task with no delay.B, Errors to criterion when delays of 10 or 20 sec were imposed. PFC, pre-frontal cortex; PTC, posterior temporal cortex.

rect platform. Their trajectory was in the general di-rection of the correct stimulus but they were less ac-curate, and thus took more time as they had to correcttheir heading near the platform.

ANOVA on the errors over the 10 trial blocks wasnot significant [^3,24) = 1.36,/? = 0.28], but ANOVAon the latency was significant [^3,24) = 5.2, p =0.006]. Post hoc comparisons (ps < 0.05) of the la-tency data showed that the parietal and prefrontalgroups had longer latencies than the control group,and the parietal group was slower than the temporalgroup. No other comparisons were significant.

DiscussionIt has been 20 years since it was first shown that ratshad a prefrontal cortex that had functional parallelsto that of larger-brained mammals (e.g., Divac, 1971;Kolb et al., 1974). In contrast, it is only recently thatthe functions of posterior parietal (Kolb and Walkey,1987) or posterior temporal (Dean, 1990) regionshave been investigated in rats and there is no consen-

sus yet on the functions of either region. The goal ofthe present experiments was to investigate further thefunctions of the three regions and to draw some cross-species generalizations regarding mammalian corticalorganization.

Prefrontal CortexIt now seems rather likely that all mammals have aregion of cortex that is functionally analogous (if nothomologous) to the prefrontal cortex of primates(e.g., Kaas, 1987; Kolb, 1990a), although the commonfunction of this region is far from settled. We wish toaddress two specific questions. First, why do frontalcortex lesions produce impairments on spatial tasks?Second, is there a general role of the prefrontal cortexin visual recognition memory? We consider these inturn.

Maze Learning and Spatial GuidanceOn the basis of studies of brain-injured war veterans,Semmes and Teuber (Semmes et al., 1963; Teuber,1964) concluded that frontal lobe lesions produced adeficit in personal orientation and that this deficit wasdissociable from a deficit in extrapersonal orientationthat was characteristic of patients with more posteriorlesions. This idea proved extremely influential andthere have been claims of a parallel distinction in non-humans as well (e.g., PohJ, 1973). It is far from clearjust what the deficit in spatial tasks may be due to,however. It could be due to an inability to learn spatialrelationships necessary to form some sort of cognitivemap of the environment, an inability to guide move-ments in space, an inability to remember spatial infor-mation necessary to guide spatial movements or toform cognitive maps, or some general deficit in adopt-ing appropriate strategies to learn the mazes. We haveseveral reasons to believe that the problem is not oneof learning spatial relationships but rather may be dueto one, or all, of the other possibilities.

First, although subsequent studies of human sub-jects with frontal lobe excisions have shown deficitsin spatial mazes, the deficits often appear to be non-spatial in nature (Corkin, 1965; Milner, 1965). For ex-ample, in both Corkin's and Milner's experiments the


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Table 3Summary of performance of rats with prefrontal, posterior parietal, or tem-poral lesions on spatial tasks

Group

Task PFC PPC PTC

Morris water taskLandmark water taskEgocentric RAMOltonRAMLashley III

NA

NA

X indicates impairment; — indicates no impairment relative to unoperatedcontrol rats; NA, not assessed. RAM, radial arm maze. Data are from Thomasand Weir 0975), Kolb et al. (1383), Kolb and Walkey (1387), DiMattia andKesner (1388a,b), Davis and McDaniel (1393), and McDamel and Skeel (1333)

patients appeared to have deficits in adopting the cor-rect strategy to solve the mazes. In fact, the subjectswere impulsive and perseverative on the tasks andMilner (1965) concluded that it was this aspect thatwas most problematic, rather than the spatial com-ponent of the tasks. Furthermore, frontal lobe patientsare not impaired at tests of spatial rotation or spatialmanipulation (de Renzi, 1982), which again speaksagainst a specific spatial integrative function. Second,although rats with medial prefrontal lesions are im-paired at the performance of virtually every task inwhich they must learn to navigate through space (Ta-ble 3), there is little direct evidence that it is a deficitin spatial guidance that is the root of the problem.Indeed, although we found rats to be impaired in theMorris task, the landmark task, and the egocentric ra-dial arm task in the present studies, we also found thata major part of their problem may be in developingan appropriate strategy to solve the task. For example,when we pretrained the animals to find a visible plat-form, their subsequent deficit in the Morris maze wasrather small. Furthermore, it has been shown that thedeficit in the Morris task is only observed in acquisi-tion, and not in retention (Sutherland, 1985). This sug-gests that animals can navigate in space in the absenceof the prefrontal cortex, provided they have alreadylearned an appropriate strategy. Indeed, we also haveseen that rats with neonatal prefrontal removals canalso learn spatial mazes as well as control animals,which again suggests that the prefrontal cortex is notessential for spatial navigation (e.g., Kolb and Whi-shaw, 1981; Sutherland et al., 1982). We must note,however, that rats with frontal lesions are sometimesimpaired at retention of spatial mazes (e.g., Becker etal., 1980; present egocentric maze results).These tasksoften confound temporal memory with spatial guid-ance, however, which makes interpretation problem-atic. In addition, frontal rats tend to perseverate ratherseverely In the performance of spatial mazes (e.g.,Kolb et al., 1974; present egocentric maze), which issimilar to Milner's patients. Finally, although eye move-ments are unlikely to play a major role in controllingspatial movements in rats, it is more likely that im-pairments in eye movements could interfere with theorganization of movements in space, and it has been

Table 4Summary of performance of rats with prefrontal, posterior parietal, or tem-poral cortex lesions on delay-type tasks

Group

Task

Delayed responseDelayed alternation

Aggleton nonmatch to sampleNo delayDelay

Mumby nonmatch to sampleKesner item recognition

PFC

XX

_

X

X

PPC

NANA

_—

z

PTC

NANA

XX

NA

X indicates impairment; — indicates no impairment relative to unoperatedcontrol rats; NA, not assessed. Data are from Kolb et al. (1974), Larsen andDrvac (1978), van Haaren et al. (1385), and Kesner and Hdbrook (1387).

proposed that one reason for spatial guidance deficitsin frontal monkeys is because of damage to visualsearch strategies and patterns (e.g., Latto, 1978; Tra-verse and Latto, 1986).

In summary, although it is clear that prefrontal le-sions impair the performance of subjects on tests ofspatial orientation and/or navigation, there is no com-pelling evidence of a unique spatial guidance functionof the prefrontal cortex. We suspect that like frontal-lobe patients, rats with prefrontal lesions are impairedat spatial mazes either because they fail to organizetheir behaviors appropriately or because of a difficultywith temporary memory of spatial information that isnecessary to form spatial "maps" (see also Winocurand Moscovitch, 1990).

Recognition MemoryJacobsen (1935) first showed that removal of the pre-frontal cortex of primates led to severe impairmentsin delayed response tasks. This result has been con-firmed repeatedly and shown in other species (Brut-kowski, 1965; Fuster, 1989; Kolb, 1990a) but the pre-cise role of the prefrontal cortex is far from settled.Nonetheless, evidence is now accumulating that dif-ferent recognition deficits may accompany lesions todifferent prefrontal regions. For example, whereas le-sions in the region of sulcus principalis would seemto produce deficits in spatial working memory (e.g.,Funahashi et al , 1993), ventromedial prefrontal lesionsproduce deficits in visual object recognition memory(e.g., Kowalska et al., 1991).

In the rat, damage to the prefrontal cortex disruptsboth acquisition and retention of a variety of tasks(sec Table 4) including delayed response (Kolb et al.,1974), delayed alternation (e.g., Wikmark et al., 1973),different types of delayed nonmatching-to-sampletasks (Dunnett, 1990; Otto and Eichenbaum, 1992;present study), and other related tasks (e.g., Kesnerand Holbrook, 1987). One interesting aspect of thepresent experiments is that the frontal rats had nodifficulty in learning the Aggleton task without a delaybut once a delay was imposed during which the stim-ulus was no longer visible, the animals were severer)'

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impaired. [Recently, Shaw and Aggleton (1993) report-ed that medial prefrontal lesions did not impair ac-quisition of the Aggleton task, but these authors didnot impose a delay in which the stimulus was notpresent.] Curiously, however, we did not find a deficitin Mumby's task. One possibility for this discrepancymight be that the only solution to the Aggleton taskis to use visual cues whereas it is possible to solve theMumby task by using the olfactory characteristics ofthe objects. That is, the objects in the Mumby taskswere distinctly different visually but they were alsodifferent olfactorily as they included metal, varioustypes of plastics, rubbers, and paints, as well as wood.Hence, since the medial prefrontal cortex receives vi-sual, but not olfactory, input it might be expected thatmedial lesions would only disrupt visually guided de-lay tasks. Rats with medial prefrontal lesions mighttherefore have solved the task using olfactory ratherthan visual cues. A corollary of this proposition is thatsince the orbital prefrontal region receives olfactoryinput, lesions to this region might produce a deficit inthe Mumby task. In fact, Otto and Eichenbaum (1992)reported a deficit in odor-guided recognition memoryin rats with orbital prefrontal lesions. Thus, there ap-pears to be at least preliminary evidence to suggestthat the prefrontal cortex of the rat may also be func-tionally subdivided with respect to its role in recog-nition memory. What has not been determined, how-ever, is whether the various regions of the medialprefrontal region might also be dissociated.

Role of the Posterior Parietal Cortex inSpatial LocalizationA principal deficit in primates with posterior parietallesions is an inability to guide the hand accurately invisual space. Thus humans or monkeys with posteriorparietal lesions make reaching errors (e.g., Hyvarinen,1982) as well as errors in visual spatial orientation(e.g., de Renzi, 1982). There are two fundamental dif-ferences in the way in which the rat guides the fore-limbs and paws in space as well as orienting the bodyin space. First, as Whishaw and Tomie (1989) haveshown, the rat does not use vision to guide the fore-limb in reaching for food. Rather, it uses its nose Sec-ond, there is a fundamental difference in the mannerin which the rat and primate visual systems are orga-nized (Goodale and Carey, 1990). The primate visualsystem is generally considered to involve two distinctstreams of visual analysis, one involved in orientationand one involved in identification (Schneider, 1969).Thus, visual recognition is assumed to involve a two-step process in which the visual stimulus is first no-ticed or localized and then is identified. Furthermore,the orientation process is assumed to involve primar-ily peripheral retina whereas the identification pro-cess primarily involves central retina. Indeed, since thecentral retina of the monkey has a 300:1 differentialin receptor density ratio from the center to the pe-riphery, it is reasonable to presume that a primate usesthe peripheral retina (and tectopulvinar visual system)to direct the central retina (and geniculostriate sys-tem) to identify visual information.

The organization is rather different in the rat, how-ever. The center/periphery ratio in the retina is onlyabout 6:1 and the ganglion cell density in the centralretina is only marginally greater than the peripheraldensity in the primate. Thus, in the rat, it is unlikely'that the act of bringing a stimulus into a position infront of the animal's head is primarily for visual iden-tification (Goodale and Carey, 1990). Rather, it is morelikely that the animal is positioning the stimulus sothat it can either explore an object using tactile orolfactory systems or locomote toward it.

The possibility that the visual organization of rat isfundamentally different from that of primates has sig-nificant implications for the organization of the pos-terior parietal region. In particular, this region is un-likely to be involved in the visual guidance of reachingor grasping with the forepaws. In addition, the poste-rior parietal region may have the main role of orient-ing the entire body toward points in space. It mightthus be expected that lesions of the posterior parietalcortex of rats would have the main effect of produc-ing a deficit in navigating through space, which is in-deed the case (Table 3) Thus, the role of the posteriorparietal region of the rat is hypothesized to be in theactive guidance of the body through visual (and per-haps tactile) space. This role would differ from that ofthe frontal cortex, which is seen as having a role inremembering the configuration of spatial cues neededto guide an animal to a previously visited location.

Comparison of the spatial navigation impairment inrats with posterior parietal and frontal lesions is in-structive in two regards. First, posterior parietal ratsare not as impaired at spatial tasks as rats with medialprefrontal lesions (or hippocampal or retrosplenial le-sions) (e.g., Sutherland et al., 1988). Second, in con-trast to rats with medial prefrontal lesions, the spatialnavigation behavior of rats with posterior parietal le-sions is consistent in that the animals are always poorat their trajectories to places and even with extendedpre- or postoperative training or extended recoveryperiods, this deficit persists.

Role of the Posterior Temporal Cortex inVisual ProcessingThe posterior temporal regions Te2 and Te3 receiveprojections from the lateral posterior nucleus andTe2/3 lesions produce deficits in certain types of vi-sual tasks (Meyer et al., 1986; Dean, 1990). Dean(1990) therefore suggested that the region might beinvolved in processing of information from peripheralvision and might therefore play some role in spatialnavigation. The results of the present study wouldseem to be inconsistent with this notion, however,since rats with large Te2/3 lesions, which includedmuch of the perirhinal cortex, performed normally inboth the Morris task and the landmark task. In con-trast, however, the posterior temporal rats were un-able to learn the Aggleton nonmatch-to-sample task,which requires a significantly different use of visualinformation than the spatial navigation tasks. Hence,in the Aggleton task the animal must process and re-tain a rather detailed representation of visual infor-

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mation to permit object identification over a short in-terval. In fact, some of the to-be-discriminated insertsin the Aggleton task are superficially quite similar, sothe animal must attend to the visual details of the stim-uli. In contrast, in the spatial navigation tasks or thevisual discrimination task, the animal is repeatedly giv-en the same visual information on every trial. In thesetasks there is no demand on a system for processingand storage of a detailed representation of novel visualinformation. Instead, a single stimulus feature (line ori-entation in the visual discrimination task) or a global,low-detail representation of spatial layout (in the nav-igation task) is sufficient to organize the correct move-ment trajectory. These results suggest that in the ratthe temporal visual cortex is necessary for a specifictype of visual identification, but is not essential forother types of visually guided performance. If thesedata prove to be generally true in further work withrats they suggest the presence of two separate pro-cessing streams for visual information. In work withprimates this idea is well established (Ungerleider andMishkin, 1982; Mishkin et al., 1983; Horwitz et al.,1992). The primate workers hypothesize that there isan occipitotemporal pathway specialized for objectidentification and an occipitoparietal pathway spe-cialized for visual guidance of movements to points inspace. We suggest that this dissociation exists in ro-dents as well as primates.

The unimpaired performance of our rats with tem-poral cortex damage on the Mumby task would seemto be at odds with our hypothesis. Although the ar-gument is purely post hoc, it is possible that as weproposed for the prefrontal rats, the temporal rats didnot use visual cues to solve the task but rather usedodors. Importantly, Mumby and Pinel (1994) have re-ported impaired performance in the Mumby task afterbilateral aspirations that included perirhinal cortexand portions of temporal neocortex and entorhinalcortex. Thus, removal of a greater extent of temporaland rhinal tissue may be necessary to interfere withperformance in this task. The bases for differences be-tween performance in the Aggleton and Mumby tasksawait future work.

Finally, we must address the role of the rhinal cortexin visually based learning in the rat. Monkeys withperirhinal lesions are severely' impaired at various testsof visual learning and memory (Zola-Morgan et al.,1989; Meunier et al., 1990). One possible reason forthis deficit is that the perirhinal/parahippocampal re-gion is a major source of entorhinal afferents, whichsubsequently informs the hippocampal formation(Deacon et al., 1983; McNaughton et al., 1989). Dea-con et al. (1983) have suggested that the perirhinalcortex of the rat is analogous to the monkey's peri-rhinal cortex and the cortex in the posterior parahip-pocampal gyrus immediately caudal to the termina-tion of the rhinal sulcus. There are two problems withthis view that critical visual information cascadesthrough temporal cortex, perirhinal/parahippocampalcortex, entorhinal cortex, to the hippocampus. Thefirst is that an absolutely fundamental contribution ofthe hippocampus is to place memory'. Yet perirhinal

damage does not impair place learning in the Morriswater task (Wigg and Bilkey, 1992; present results).Second, there is no clear experimental evidence in rator monkey that damage specifically to the hippocam-pus causes an important impairment in object-basedvisual recognition memory (Aggleton et al., 1986, Kes-ner, 1991; Rothblat and Kromer, 1991; Mumby et al.,1992). An alternative to the cascade of visual infor-mation described above holds that the separation ofdorsal and ventral visual processing streams is morethoroughgoing than is currently supposed. Instead ofthe ventral, detailed object-processing system beingreintegrated with the dorsal, spatial movement systemin the hippocampal formation, these two remain sep-arate. On this view, the hippocampus and entorhinaland posterior cingulate cortex are critical for placememory but make a nonessential contribution to ob-ject memory, and the rhinal and temporal cortex arecritical for object memory but make a nonessentialcontribution to place memory. Furthermore, concep-tually it would seem counterproductive for there tobe anatomically distinct processing channels to em-phasize processing of different dimensions of the vi-sual array only to have these reintegrate in a corticalregion specialized for memory.

Cross-Species ConclusionsThe results of the present experiments are consistentwith the general idea that the mammalian neocortexhas three distinct regions of "association cortex" thatare functionally dissociable. First, there is a prefrontalregion whose general functions appear to be generallysimilar across a wide variety of mammalian species(e.g., Fuster, 1989; Kolb, 1984,1990a). We have arguedelsewhere that this apparent similarity in mammalianprefrontal function reflects the general requirementsof temporally organizing behaviors in animals with be-havior repertoires that are far more plastic than thoseof other classes of animals, such as birds or reptiles(e.g., Kolb, 1990a). Nonetheless, the anatomical par-cellation of subareas is significantly different acrossspecies, and it is likely that as the functional proper-ties of the subareas are explored there will be signif-icant interspecies differences in the details of prefron-tal organization.

Second, there is a posterior parietal region of mam-mals that plays some role in the visuospatial guidanceof behavior. It is our view, however, that the develop-ment of the posterior parietal area is correlated withthe development of foveal vision. Thus, animals likerats who have poor foveal vision, relative to peripheralvision, will have a modest posterior parietal region rel-ative to more visual animals like primates. For the rat,the function of this cortex is to orient the body, andparticularly the snout, toward points in space.

Finally, there is a posterior temporal region that hassome role in visual learning. In view of the absenceof deficits in visual spatial learning, or in simple dis-crimination learning, we believe that this area likelyhas some general role in object identification in mam-mals.

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NotesThis research was supported by a Natural Science and En-gineering Research Council of Canada grant to B.K We thankBrigittc Byers for cutting the brains, Robbin Gibb for help invarious aspects of the behavioral testing, and Jan Cioe forhelpful comments on the manuscript.

Correspondence should be addressed to Bryan Kolb, De-partment of Psychology, University of Lethbridge, Lethbridge,AB, Canada, T1K 3M4.

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