The Parahippocampal Region and Object Identification

E.A. MURRAY,a T.J. BUSSEY, R.R. HAMPTON, AND L.M. SAKSIDA Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892, USA

ABSTRACT: The hippocampus has long been thought to be critical for memory, including memory for objects. However, recent neuropsychological studies in nonhuman primates have indicated that other regions within the medial temporal lobe, specifically, structures in the parahippocampal region, are prima- rily responsible for object recognition and object identification. This article reviews the behavioral effects of removal of structures within the parahippocampal region in monkeys, and cites relevant work in rodents as well. It is ar- gued that the perirhinal cortex, in particular, contributes to object identification in at least two ways: (i) by serving as the final stage in the ventral visual cortical pathway that represents stimulus features, and (ii) by operating as part of a network for associating together sensory inputs within and across sensory modalities.

INTRODUCTION

This article reviews the contributions of the parahippocampal region to learning and memory in nonhuman primates, with special emphasis on its role in object identification: the knowledge that a particular object or class of objects is one and the same across the different instances in which it is experienced. In macaque monkeys, the parahippocampal region consists of three main cortical fields, located on the ven- tromedial aspect of the temporal lobe: entorhinal cortex, perirhinal cortex, and parahippocampal cortex (see FIG. 1). Currently, much more information is available regarding the contributions of the perirhinal cortex to learning and memory than for either the entorhinal cortex or parahippocampal cortex. Accordingly, although future studies might consider whether the functions of the cortical fields comprising the parahippocampal region can be understood within a unified framework, the present article focuses on the functions of just one portion of this region, namely, the perirhinal cortex. We cover two main topics. First, we discuss the specific behavioral impairments that follow ablations of perirhinal cortex in macaque monkeys. Parallel findings in rats are also noted. Second, taking into account the results from these ablation studies, we discuss a tentative framework for understanding many of the behavioral effects of perirhinal cortex removal. Finally, we briefly summarize the contributions

aAddress for correspondence: Elisabeth A. Murray, Ph.D., Laboratory of Neuropsychology, National Institute of Mental Health, Building 49, Room 1B80, 49 Convent Drive, Bethesda, MD 20892-4415. Tel.: (301) 496-5625, ext. 227; fax: (301) 402-0046. e-mail: [email protected]

166 MURRAY et al.: OBJECT IDENTIFICATION 167 of the perirhinal cortex to visual perception and memory, and the way in which these promote object identification.

WHAT BEHAVIORAL IMPAIRMENTS FOLLOW DAMAGE TO THE PARAHIPPOCAMPAL REGION?

One of the earliest reported deficits found after damage to the parahippocampal region was an impairment in visual object recognition memory, as measured by the delayed nonmatching-to-sample (DNMS) or delayed matching-to-sample (DMS) tasks. In DNMS, each trial has two parts: a sample presentation followed by a choice test. During the sample presentation, the monkey sees a single object, which covers the central well of a three-well test tray. The monkey then displaces the object to obtain a small piece of food hidden in the well underneath. A few seconds later the monkey sees the same, now-familiar object plus a novel one, with one object covering the left well of the test tray and the other covering the right well. The monkey can obtain a second piece of food by displacing the novel object, but not by pushing aside the familiar one. Thus, on the choice test, the monkey solves the problem by applying a “nonmatching” rule, that is, by choosing the object that does not match the sample. If the monkey consistently chooses the novel object on the choice test, one can infer that the monkey recognizes the sample. In DMS, the monkey is trained on the “matching” rule rather than the nonmatching rule. These tasks can also be ad- ministered using a computerized apparatus that presents two-dimensional pictures on a touch-sensitive video screen rather than using actual objects on a test tray. Monkeys with combined removals of the entorhinal cortex and perirhinal cortex are severely impaired on visual DNMS1 and DMS.2 Monkeys with such lesions perform at high levels of accuracy when delay intervals between the sample presentation and choice are short (∼10 s), but perform at near chance levels when given a choice test only 60 seconds or so after presentation of the sample. By contrast, unoperated control monkeys perform over 90% correct responses at these and longer delay intervals.1 Although alternative accounts have been proposed,3 this pattern of results is traditionally interpreted as demonstrating rapid forgetting in the operated group. The precise nature of the deficit aside, these experiments show that, within the medial temporal lobe, the perirhinal cortex and the entorhinal cortex are important for visual recognition memory. The perirhinal cortex, in particular, appears to play a central role in visual recognition. Within the parahippocampal region, ablation or reversible cooling of this cortical field yields the most devastating effects on visual recognition memory.1,4,5 Removals restricted to the entorhinal cortex yield only mild, transient deficits on visual recognition.1,6 Preliminary data indicate that removals restricted to the parahippocampal cortex yield no deficits.7 Finally, even though ablations of entorhinal cortex alone produce little or no disruption of visual recognition, circumstantial evidence suggests that the entorhinal cortex, as well as area TE (a cortical field just lat- eral to the perirhinal cortex), can contribute to visual recognition. Monkeys with combined damage either to the entorhinal cortex plus perirhinal cortex, or to area TE plus the perirhinal cortex, have greater recognition impairments than do monkeys with damage to the perirhinal cortex alone.8 Importantly, these group differences in the magnitude of the recognition impairment cannot be accounted for by differences 168 ANNALS NEW YORK ACADEMY OF SCIENCES

FIGURE 1. Diagrams of the medial (A) and ventral (B) views of the right hemisphere of a macaque brain showing the location and extent of various structures in the medial temporal lobe. The amygdala and the hippocampus are buried deep within the temporal lobe, whereas the perirhinal, entorhinal, and parahippocampal cortical fields are located on the surface of the brain. across groups in the size of the perirhinal cortex removal itself, indicating that the cortex outside the perirhinal field is indeed making a contribution. Impairments in recognition memory after combined damage to the perirhinal and entorhinal cortex have now been reported under several different conditions. For example, impairments are found in studies using either DNMS or DMS tasks in monkeys, using either a manual1 or an automated2 test apparatus, and using either visual9 MURRAY et al.: OBJECT IDENTIFICATION 169 or olfactory10 versions of DNMS in rats. In addition, monkeys with removals of perirhinal plus parahippocampal cortex are impaired on a tactual version of DNMS.11 Selective perirhinal cortex damage can also affect tactual DNMS.5 Thus, the recognition impairment after perirhinal cortex damage is robust, and affects more than one sensory modality. Currently, there is controversy about the way in which various medial temporal lobe structures (including the entorhinal cortex, perirhinal cortex, parahippocampal cortex, amygdala and hippocampus) contribute to visual recognition memory. Al- though there is widespread agreement that the perirhinal and entorhinal cortex play a central role in recognition memory, and also that the amygdala is not important for this type of memory, no such consensus of opinion exists about the potential contribution of the hippocampus. Many studies have reported that damage to the hippocampus or fornix produces little or no impairment on visual recognition. For example, such damage produces either a mild impairment or no impairment on visual DNMS in monkeys,12–14 as well as on olfactory10 or visual recognition memory tasks9,15–17 in rats. Recently, however, two additional studies have examined the effects of excitotoxic lesions of the hippocampus in monkeys, and both found impairments on DNMS.18,19 Two points are worth making in this regard. First, the impairment that follows hippocampal lesions, when it is found, is much milder than that which follows perirhinal and entorhinal cortex damage. Second, for the hippocampus, there is no evidence for a positive correlation between magnitude of the recognition impairment and volume of the lesion, as one would predict if a given structure were medi- ating a given function. Indeed, one study has reported a significant inverse correlation,13 and the two others likewise yielded negative correlations, although they do not attain statistical significance. By contrast, a positive correlation exists between the amount of damage to the entorhinal and perirhinal cortex, considered together, and magnitude of the recognition memory impairment.1 Although a de- tailed discussion of this set of findings is beyond the scope of this article, we note that the data are consistent with the idea that partial hippocampal lesions might yield an indirect, adverse effect on other brain structures,20,21 perhaps including the entorhinal and perirhinal cortex. In sum, damage to the hippocampus produces an impairment in visual recognition memory in some studies but not in others, and the manner in which the deficit arises remains uncertain. Recognition memory, however, is not the only function disrupted by damage to the parahippocampal region. Monkeys with lesions of the entorhinal and perirhinal cortex have been found to be impaired in the learning or retention of stimulus- stimulus associations, including visual-visual associations or “paired associates,”22 tactile-visual associations,23 and flavor-visual associations.24 In addition, rats with lesions of the entorhinal and perirhinal cortex are poor at an olfactory version of paired-associate learning.25 As was the case for visual recognition memory, it appears that, within the parahippocampal region, the perirhinal cortex is especially critical for this kind of association learning.26 Whether the perirhinal cortex is essential for all types of stimulus-stimulus associations in nonhuman primates, or only for those involving visual stimuli, remains uncertain. Future studies should address this question experimentally. As was the case for recognition, stimulus-stimulus associations can proceed in the absence of the hippocampus. For example, learning of visual–visual associations22 and retention of tactual-visual associations27 in monkeys is unaffect- 170 ANNALS NEW YORK ACADEMY OF SCIENCES ed by hippocampal removals. Although there are no studies assessing the effects of removal of the parahippocampal cortex alone, both studies cited above used aspira- tion removals of the hippocampus that included the underlying parahippocampal cortex. Thus, it is unlikely that selective removals of the parahippocampal cortex would disrupt this kind of stimulus-stimulus associative learning. A third class of task on which there are impairments after removals within the parahippocampal region is pair-wise discrimination learning. Lesions of the perirhinal cortex alone, or of the entorhinal and perirhinal cortex together, have yielded mixed results; in some cases no impairment has been found,2,28–30 and, in others, impairments have been reported.5,30–32 Buckley and Gaffan30 conducted a study to test the possibility that the deficits in concurrent visual discrimination learning following perirhinal cortex removals were related to the number of items to be discriminated (i.e., stimulus set size). Although the results as reported appear somewhat equivocal, a reanalysis restricted to the data from novel discriminations reveals stronger evidence for a relationship between set size and the magnitude of the deficit. These results thus lend some support to the hypothesis that the number of items to be discriminated is a factor underlying the impairments in concurrent discrimination learning. Another type of impairment in discrimination learning observed after perirhinal cortex removal is a severe deficit in configural discrimination learning,26 even when small stimulus sets are used. Finally, either removals of the perirhinal plus entorhinal cortex, or removals of the perirhinal cortex alone, have been reported to disrupt retention of preoperatively learned discrimination problems in both monkeys28,29,32 and rats.33–35

WHAT ARE THE CONTRIBUTIONS OF THE PARAHIPPOCAMPAL REGION TO PERCEPTION AND MEMORY?

As we have seen, perirhinal cortex lesions produce a variety of effects on visual learning and memory tasks, and yield some disruption in cross-modal associative tasks as well. Recently, Saksida and Bussey36 have suggested that many of the effects of perirhinal cortex lesions described above may be understood by a consider- ation of the organization of visual representations in inferior temporal cortex, including the perirhinal cortex. Specifically, it has been proposed36,37 that as one proceeds rostrally within the ventral visual processing stream, or “what” pathway, neurons code stimulus representations of increasing complexity. On this view, neurons in perirhinal cortex (and perhaps entorhinal cortex) represent complex conjunctions of features of visual stimuli, whereas neurons in earlier regions in the visual processing pathway represent simpler features from which the conjunctions are formed. This view is supported by anatomical and electrophysiological studies, which suggest a hierarchical organization of visual information processing in the inferior temporal cortex.38,39 In this sense, perirhinal cortex might be considered to be the final station in the ventral visual processing stream. If this supposition concerning the hierarchical organization of visual representations is correct, then perirhinal cortex should be particularly important for discriminations requiring the use of the complex visual representations stored there. For example, such representations would be required when the discrimination could not be solved on the basis of simple features of the discriminanda, a situation that arises MURRAY et al.: OBJECT IDENTIFICATION 171 in “configural” learning tasks. If one considers a configural task such as the bicon- ditional discrimination, AB+, CD+, BC−, AD− (where AB can be thought of as an object, A and B as features of that object, and + and − as indicating whether a given object is rewarded or not), it can easily be seen that such a discrimination cannot be solved on the basis of simple features alone: sometimes A is rewarded; sometimes it is not. However, by associating representations of the conjunctions of features such as AB with reward or nonreward, the task can be solved. Consistent with this analysis, Buckley and Gaffan26 found that perirhinal cortex lesions severely disrupted configural learning in monkeys. This analysis can also account for impairments in concurrent discrimination learning with large stimulus sets. This is because as the number of objects to be discriminated increases, the probability increases that a given feature might be rewarded in one case (i.e., one object) but not in another. A prediction that follows is that deficits in configural discriminations—in which the amount of feature ambiguity is at a maximum—should be obtainable using a smaller set size than that required to obtain impairments in concurrent discrimination learning. Although this has not been tested directly in a single experiment, comparison across studies supports this prediction.26,30 Other predictions follow from the proposal that visual representations in inferior temporal cortex are organized hierarchically. For example, in cases where the discriminanda have many visual features in common, even discrimination of a single pair of objects could be disrupted in monkeys with perirhinal cortex removals relative to controls. Preliminary results support this idea. Bussey et al.40 first taught monkeys to discriminate complex greyscale picture stimuli. By use of a computer al- gorithm, the pictures were then “morphed” (blended) together in a manner that increased the number of features the discriminanda had in common. Although perirhinal cortex lesions did not disrupt the acquisition of the original discrimination, performance in these animals was impaired, relative to controls, when the number of common features was increased. By contrast, performance of the same operated monkeys did not differ from that of controls after the same types of picture stimuli were made more difficult to discriminate, not by increasing the number of common features, but by manipulating their size. The studies reviewed above indicate an important role for the perirhinal cortex in object identification. The case for a role for perirhinal cortex in object identification has been made even stronger by the results of experiments by Buckley and Gaffan, who showed that perirhinal cortex lesions can disrupt object discrimination when objects are presented in new views, or presented within a complex scene.41 Similar findings have been reported in rodents. For example, E.A. Gaffan et al.42 found that rats with perirhinal cortex lesions had a specific difficulty in discriminating objects embedded in scenes. In their task, rats were required to discriminate a “constant negative,” nonrewarded scene from positive, rewarded scenes. In brief, when spatial cues were available, the operated rats could discriminate the scenes, but when only stimulus quality cues were available, the rats were impaired, suggesting a specific difficulty with object identification. There are, however, some limitations on the conditions under which the perirhinal cortex is essential for object identification. Re- cently, Hampton and Murray32 tested the effects of perirhinal cortex removals on various aspects of object identification, including, among other things, discrimination of rotated objects, shrunken or enlarged objects, and degraded objects presented on a monitor screen. Whereas the manipulations of the images were effective in sub- 172 ANNALS NEW YORK ACADEMY OF SCIENCES stantially increasing the difficulty of the discriminations, monkeys with perirhinal cortex removals performed at the same level of accuracy as the unoperated controls. In contrast to these negative findings, the same operated monkeys were impaired in the learning of both concurrent and single pair visual object discriminations, so the lack of impairment on the earlier tests cannot be accounted for by ineffective lesions. These results constrain the ways in which the perirhinal cortex can be said to contribute to object identification, by showing that the perirhinal cortex is not necessary for the identification and selection of familiar objects under certain challenging conditions.

SUMMARY

For the present, it appears that the perirhinal cortex contributes to object identification in at least two different ways. First, it is thought to process information in much the same way as other parts of inferior temporal cortex, and may serve as the final stage in the ventral visual processing pathway devoted to visual perception and memory. Its special contribution is held to be in the representation of complex conjunctions of stimulus features. To the extent that the perirhinal cortex serves to represent stimuli, it can be said to contribute to object identification. Second, the perirhinal cortex operates as part of a network for associating together sensory inputs within and across sensory modalities. In addition, the perirhinal cortex, together with other cortical fields, also serves as a site of long-term storage of such knowledge. Thus, the perirhinal cortex in monkeys, together with other brain regions, appears to comprise a network analogous to a semantic network in humans, specialized for rep- resenting objects and object-related information.

ACKNOWLEDGMENT

This work is supported by the Intramural Research Program of the National Institute of Mental Health.

REFERENCES

1. MEUNIER, M., J. BACHEVALIER, M. MISHKIN & E.A. MURRAY. 1993. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J. Neurosci. 13: 5418–5432. 2. EACOTT, M.J., D. GAFFAN & E.A. MURRAY. 1994. Preserved recognition memory for small sets, and impaired stimulus identification for large sets, following rhinal cortex ablations in monkeys. Eur. J. Neurosci. 6: 1466–1478. 3. RINGO, J.L. 1991. Memory decays at the same rate in macaques with and without brain lesions when expressed in d' or arcsine terms. Behav. Brain Res. 42: 123–134. 4. HOREL, J.A., D.E. PYTKO-JOINER, M.L. VOYTKO & K. SALSBURY. 1987. The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav. Brain Res. 23: 29–42. 5. BUFFALO, E.A., S.J. RAMUS, R.E. CLARK, E. TENG, L.R. SQUIRE & S.M. ZOLA. 1999. Dissociation between the effects of damage to perirhinal cortex and area TE. Learn. Memory 6: 572–599. MURRAY et al.: OBJECT IDENTIFICATION 173

6. LEONARD, B.W., D.G. AMARAL, L.R. SQUIRE & S. ZOLA-MORGAN. 1995. Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex. J. Neurosci. 15: 5637–5659. 7. RAMUS, S.J., S. ZOLA-MORGAN & L.R. SQUIRE. 1994. Effects of lesions of perirhinal cortex or parahippocampal cortex on memory in monkeys. Soc. Neurosci. Abstr. 20: 1074. 8. MURRAY, E.A. 2000. Memory for objects in nonhuman primates. In The New Cogni- tive Neurosciences. M.S. Gazzaniga, Ed.: 753–763. MIT Press. Cambridge, MA. 9. MUMBY, D.G. & J.P.J. PINEL. 1994. Rhinal cortex lesions and object recognition in rats. Behav. Neurosci. 108: 11–18. 10. OTTO, T. & H. EICHENBAUM. 1992. Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to- sample task. Behav. Neurosci. 106: 762–775. 11. SUZUKI, W.A., S. ZOLA-MORGAN, L.R. SQUIRE & D.G. AMARAL. 1993. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J. Neurosci. 13: 2430–2451. 12. BACHEVALIER, J., R.C. SAUNDERS & M. MISHKIN. 1985. Visual recognition in monkeys: effects of transection of fornix. Exp. Brain Res. 57: 547–553. 13. MURRAY, E.A. & M. MISHKIN. 1998. Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J. Neurosci. 18: 6568–6582. 14. GAFFAN, D. 1994. Dissociated effects of perirhinal cortex ablation, fornix transection and amygdalectomy: evidence for multiple memory systems in the primate temporal lobe. Exp. Brain Res. 99: 411–422. 15. ROTHBLAT, L.A. & L.F. KROMER. 1991. Object recognition memory in the rat: the role of the hippocampus. Behav. Brain Res. 42: 25–32. 16. STEELE, K. & J.N.P. RAWLINS. 1993. The effects of hippocampectomy on performance by rats of a running recognition task using long lists of non-spatial items. Behav. Brain Res. 54: 1–10. 17. BUSSEY, T.J., J. DUCK, J.L. MUIR & J.P. AGGLETON. 2000. Distinct patterns of behav- ioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav. Brain Res. In press. 18. BEASON-HELD, L.L., D.L. ROSENE, R.J. KILLIANY & M.B. MOSS. 1999. Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 9: 562–574. 19. ZOLA, S.M., L.R. SQUIRE, E. TENG, L. STEFANACCI, E.A. BUFFALO & R.E. CLARK. 2000. Impaired recognition memory in monkeys after damage limited to the hippocampal region. J. Neurosci. 20: 451–463. 20. BACHEVALIER, J. & M. MISHKIN. 1989. Mnemonic and neuropathological effects of occluding the posterior cerebral artery in Macaca mulatta. Neuropsychologia 27: 83–105. 21. MISHKIN, M. & E.A. MURRAY. 1994. Stimulus recognition. Curr. Opin. Neurobiol. 4: 200–206. 22. MURRAY, E.A., D. GAFFAN & M. MISHKIN. 1993. Neural substrates of visual stimulus- stimulus association in rhesus monkeys. J. Neurosci. 13: 4549–4561. 23. GOULET, S. & E.A. MURRAY. 1995. Effects of lesions of either the amygdala or anterior rhinal cortex on crossmodal DNMS in rhesus macaques. Soc. Neurosci. Abstr. 21: 1446. 24. PARKER, A. & D. GAFFAN. 1998. Lesions of the primate rhinal cortex cause deficits in flavour-visual associative memory. Behav. Brain Res. 93: 99–105. 25. BUNSEY, M. & H. EICHENBAUM. 1993. Critical role of the parahippocampal region for paired-associate learning in rats. Behav. Neurosci. 107: 740–747. 26. BUCKLEY, M.J. & D. GAFFAN. 1998. Perirhinal cortex ablation impairs configural learning and paired–associate learning equally. Neuropsychologia 36: 535–546. 27. MURRAY, E.A. & M. MISHKIN. 1985. Amygdalectomy impairs crossmodal association in monkeys. Science 228: 604–606. 28. GAFFAN, D. & E.A. MURRAY. 1992. Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. Behav. Neurosci. 106: 30–38. 174 ANNALS NEW YORK ACADEMY OF SCIENCES

29. THORNTON, J.A., L.A. ROTHBLAT & E.A. MURRAY. 1997. Rhinal cortex removal produces amnesia for preoperatively learned discrimination problems but fails to disrupt postop- erative acquisition and retention in rhesus monkeys. J. Neurosci. 17: 8536–8549. 30. BUCKLEY, M.J. & D. GAFFAN. 1997. Impairment of visual object-discrimination learning after perirhinal cortex ablation. Behav. Neurosci. 111: 467–475. 31. BAXTER, M.G., W.S. HADFIELD & E.A. MURRAY. 1999. Rhinal cortex lesions produce mild deficits in visual discrimination learning for an auditory secondary reinforcer in rhesus monkeys. Behav. Neurosci. 113: 243–252. 32. HAMPTON, R.R. & E.A. MURRAY. 1999. Stimulus representations in rhesus monkeys with perirhinal cortex lesions. Soc. Neurosci. Abstr. 25: 789–789. 33. WIIG, K.A., L.N. COOPER & M.F. BEAR. 1996. Temporally graded retrograde amnesia following separate and combined lesions of the perirhinal cortex and fornix in the rat. Learn. Memory 3: 313–325. 34. KORNECOOK, T.J., A. ANZARUT & J.P.J. PINEL. 1999. Rhinal cortex, but not medial thalamic, lesions cause retrograde amnesia for objects in rats. Neuroreport 10: 2853–2858. 35. MACHIN, P.E. & M.J. EACOTT. 1999. Perirhinal cortex and visual discrimination learning in the rat. Psychobiology 27: 470–479. 36. SAKSIDA, L.M. & T.J. BUSSEY. 1998. Toward a neural network model of visual object identification in primate inferotemporal cortex. Soc. Neurosci. Abstr. 24: 1906. 37. MURRAY, E.A. & T.J. BUSSEY. 1999. Perceptual-mnemonic functions of the perirhinal cortex. Trends Cognit. Sci. 3: 142–151. 38. TANAKA, K. 1996. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19: 109–139. 39. LOGOTHETIS, N.K. 1998. Object vision and visual awareness. Curr. Opin. Neurobiol. 8: 536–544. 40. BUSSEY, T.J., L.M. SAKSIDA & E.A. MURRAY. 1999. Overgeneralization in monkeys with perirhinal cortex lesions. Soc. Neurosci. Abstr. 25: 789. 41. BUCKLEY, M.J. & D. GAFFAN. 1998. Perirhinal cortex ablation impairs visual object identification. J. Neurosci. 18: 2268–2275. 42. GAFFAN, E.A., M.J. EACOTT & E.L. SIMPSON. 2000. Perirhinal cortex ablation in rats selectively impairs object identification in a simultaneous visual comparison task. Behav. Neurosci. 114: 18–31.