Identifying cortical inputs to the rat hippocampus that subserve allocentric spatial processes: A simple problem with a complex answer

A consideration of the cortical projections to the hippocampus provides a number of candidate regions that might provide distal sensory information needed for allocentric processing. Prominent among the input regions are the entorhinal cortex, the perirhinal cortex, the postrhinal cortex, and the retrosplenial cortex. A review of these sites reveals the surprising fact that in spite of their anatomical connections, removal of the perirhinal and postrhinal cortices has little or no effect on spatial tasks and hence does not functionally disconnect the hippocampus. Extensive retrosplenial lesions have only mild effects, and even lesions of the entorhinal cortex only partially mimic the effects of hippocampal lesions upon tests of spatial memory. In contrast, studies using c‐fos imaging support the involvement of the entorhinal, postrhinal, and retrosplenial cortices, but not the perirhinal cortex. It is argued that there exist multiple aspects of spatial memory, and this is reflected in the multiple routes by which cortical information can reach the hippocampus. One consequence is that lesions in a single site often have surprisingly mild effects on standard spatial tests. Hippocampus 10:466–474, 2000 © 2000 Wiley‐Liss, Inc.

[1]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[2]  J. Aggleton,et al.  The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat , 1997, Behavioural Brain Research.

[3]  J. Michael Wyass,et al.  Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review , 1992, Hippocampus.

[4]  R. J. McDonald,et al.  Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. , 1994, Cerebral cortex.

[5]  J M Wyss,et al.  Connections of the retrosplenial dysgranular cortex in the rat , 1992, The Journal of comparative neurology.

[6]  The effect of excitotoxic lesions centered on the perirhinal cortex in two versions of the radial arm maze task. , 1999, Behavioral neuroscience.

[7]  T. Bussey,et al.  Functionally Dissociating Aspects of Event Memory: the Effects of Combined Perirhinal and Postrhinal Cortex Lesions on Object and Place Memory in the Rat , 1999, The Journal of Neuroscience.

[8]  M. J. Kiernan,et al.  Microinjection of morphine into the nucleus accumbens impairs contextual learning in rats , 1997 .

[9]  D. Pandya,et al.  Some observations on the course and composition of the cingulum bundle in the rhesus monkey , 1984, The Journal of comparative neurology.

[10]  N. Neave,et al.  Evidence for the Involvement of the Mammillary Bodies and Cingulum Bundle in Allocentric Spatial Processing by Rats , 1997, The European journal of neuroscience.

[11]  Acquisition of a complex place task in rats with selective ibotenate lesions of hippocampal formation: combined lesions of subiculum and entorhinal cortex versus hippocampus. , 1988, Behavioral neuroscience.

[12]  G. Higgins,et al.  Characterization of perforant path lesions in rodent models of memory and attention , 1998, The European journal of neuroscience.

[13]  J. Rawlins,et al.  The effects of NMDA‐induced retrohippocampal lesions on performance of four spatial memory tasks known to be sensitive to hippocampal damage in the rat , 1999, The European journal of neuroscience.

[14]  J. Aggleton,et al.  Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat , 1994, Behavioural Brain Research.

[15]  I. Whishaw Place Learning in Hippocampal Rats and the Path Integration Hypothesis , 1998, Neuroscience & Biobehavioral Reviews.

[16]  Dave G. Mumby,et al.  Place memory is intact in rats with perirhinal cortex lesions. , 1998 .

[17]  T. Bussey,et al.  Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat , 2000, Behavioural Brain Research.

[18]  W. Tischmeyer,et al.  Activation of immediate early genes and memory formation , 1999, Cellular and Molecular Life Sciences CMLS.

[19]  M. W. Brown,et al.  Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel environment , 1997, Neuroscience Letters.

[20]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[21]  N. Schmajuk,et al.  Stimulus configuration, classical conditioning, and hippocampal function. , 1992, Psychological review.

[22]  M. Gluck,et al.  Dissociation of hippocampal and entorhinal function in associative learning: A computational approach , 1995, Psychobiology.

[23]  J. J. Hagan,et al.  Behavioural and electrophysiological studies of entorhinal cortex lesions in the rat , 1992, Physiology & Behavior.

[24]  J. Aggleton,et al.  Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat , 1996, Behavioural Brain Research.

[25]  J. Aggleton,et al.  Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix , 1997, Experimental Brain Research.

[26]  R. C. Honey,et al.  Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. , 1997, Behavioral neuroscience.

[27]  T. Bussey,et al.  Extensive Cytotoxic Lesions Involving Both the Rhinal Cortices and Area TE Impair Recognition But Spare Spatial Alternation in the Rat , 1997, Brain Research Bulletin.

[28]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[29]  J. Aggleton,et al.  A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  C. Hölscher,et al.  Quinolinic acid lesion of the rat entorhinal cortex pars medialis produces selective amnesia in allocentric working memory (WM), but not in egocentric WM , 1994, Behavioural Brain Research.

[31]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[32]  M. Witter,et al.  Parallel input to the hippocampal memory system through peri‐ and postrhinal cortices , 1997, Neuroreport.

[33]  D L Rosene,et al.  A comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: I. Convergence in the entorhinal, prorhinal, and perirhinal cortices , 1988, The Journal of comparative neurology.

[34]  R. Morris,et al.  Ibotenate Lesions of Hippocampus and/or Subiculum: Dissociating Components of Allocentric Spatial Learning , 1990, The European journal of neuroscience.

[35]  J. Cassel,et al.  Spatial memory, habituation, and reactions to spatial and nonspatial changes in rats with selective lesions of the hippocampus, the entorhinal cortex or the subiculum , 1998, Behavioural Brain Research.

[36]  M. W. Brown Neuronal responses and recognition memory , 1996 .

[37]  M. W. Brown,et al.  Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain , 1995, Neuroscience.

[38]  R. Burwell,et al.  Memory impairment on a delayed non-matching-to-position task after lesions of the perirhinal cortex in the rat. , 1998, Behavioral neuroscience.

[39]  K A Wiig,et al.  Perirhinal cortex lesions in rats disrupt performance in a spatial DNMS task , 1994, Neuroreport.

[40]  M. Gabriel,et al.  Neurobiology of Cingulate Cortex and Limbic Thalamus , 1993 .

[41]  R. Sutherland,et al.  Contributions of cingulate cortex to two forms of spatial learning and memory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  R. J. McDonald,et al.  Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. , 1994, Behavioral and neural biology.

[43]  J. Aggleton,et al.  The effects of discrete cingulum bundle lesions in the rat on the acquisition and performance of two tests of spatial working memory , 1996, Behavioural Brain Research.

[44]  D. Bilkey,et al.  The effects of perirhinal cortical lesions on spatial reference memory in the rat , 1994, Behavioural Brain Research.

[45]  John M. Pearce,et al.  Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors , 1998, Nature.

[46]  T. Herdegen,et al.  Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins , 1998, Brain Research Reviews.

[47]  L. Jarrard,et al.  Effects of Postoperative Housing Conditions on Functional Recovery in Rats with Lesions of the Hippocampus, Subiculum, or Entorhinal Cortex , 1997, Neurobiology of Learning and Memory.

[48]  R. Sutherland,et al.  Posterior Cingulate Cortex and Spatial Memory: A Microlimnology Analysis , 1993 .

[49]  D. Amaral,et al.  Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 1998 .

[50]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

[51]  R. Kesner,et al.  Neural circuit analysis of spatial working memory: Role of pre‐ and parasubiculum, medial and lateral entorhinal cortex , 1998, Hippocampus.

[52]  H Eichenbaum,et al.  Afferent connections of the perirhinal cortex in the rat , 1983, The Journal of comparative neurology.

[53]  R. Morris Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

[54]  J. Rawlins,et al.  Cytotoxic lesions of the retrohippocampal region attenuate latent inhibition but spare the partial reinforcement extinction effect , 1997, Experimental Brain Research.

[55]  V. B. Domesick The fasciculus cinguli in the rat. , 1970, Brain research.

[56]  R. Sutherland,et al.  The role of the fornix/fimbria and some related subcortical structures in place learning and memory , 1989, Behavioural Brain Research.

[57]  J. T. Erichsen,et al.  Fos Imaging Reveals Differential Patterns of Hippocampal and Parahippocampal Subfield Activation in Rats in Response to Different Spatial Memory Tests , 2000, The Journal of Neuroscience.

[58]  J. Barnes,et al.  Evidence for recovery of spatial learning following entorhinal cortex lesions in mice , 1997, Brain Research.

[59]  Malcolm W. Brown,et al.  Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory , 1999, The Journal of Neuroscience.

[60]  M. Max,et al.  Effects of a Postoperative , 1992 .

[61]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[62]  J. Aggleton,et al.  Assessing the magnitude of the allocentric spatial deficit associated with complete loss of the anterior thalamic nuclei in rats , 1997, Behavioural Brain Research.

[63]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[64]  M. M. Glasier,et al.  Effects of Unilateral Entorhinal Cortex Lesion and Ganglioside GM1 Treatment on Performance in a Novel Water Maze Task , 1995, Neurobiology of Learning and Memory.

[65]  Barbara J. Knowlton,et al.  Memory, hippocampus, and brain systems. , 1995 .

[66]  B. Vogt,et al.  Form and distribution of neurons in rat cingulate cortex: Areas 32, 24, and 29 , 1981, The Journal of comparative neurology.

[67]  D. G. Herrera,et al.  Activation of c-fos in the brain , 1996, Progress in Neurobiology.

[68]  R. Faull,et al.  The use of c-fos as a metabolic marker in neuronal pathway tracing , 1989, Journal of Neuroscience Methods.

[69]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[70]  J. Muir,et al.  Comparing the effects of selective cingulate cortex lesions and cingulum bundle lesions on water maze performance by rats , 1998, The European journal of neuroscience.

[71]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

[72]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[73]  J. Aggleton,et al.  The contribution of the anterior thalamic nuclei to anterograde amnesia , 1993, Neuropsychologia.

[74]  A. Dickinson,et al.  Episodic memory: what can animals remember about their past? , 1999, Trends in Cognitive Sciences.

[75]  M. Good,et al.  The effects of combined lesions of the subicular complex and the entorhinal cortex on two forms of spatial navigation in the water maze. , 2000, Behavioral neuroscience.

[76]  E. Coutureau,et al.  Entorhinal but Not Hippocampal or Subicular Lesions Disrupt Latent Inhibition in Rats , 1999, Neurobiology of Learning and Memory.