Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory.

Despite the connections of the retrosplenial cortex strongly suggesting a role in spatial memory, the lesion data to date have been equivocal. Whether subjects are impaired after retrosplenial lesions seems to depend on whether the lesions were aspirative or excitotoxic, with the latter failing to produce an impairment. A shortcoming of previous excitotoxic lesion studies is that they spared the most caudal part of the retrosplenial cortex. The present study thus used rats with extensive neurotoxic lesions of the retrosplenial cortex that encompassed the entire rostrocaudal extent of this region. These rats were consistently impaired on several tests that tax allocentric memory. In contrast, they were unimpaired on an egocentric discrimination task. Although the lesions did not appear to affect object recognition, clear deficits were found for an object-in-place discrimination. The present study not only demonstrates a role for the retrosplenial cortex in allocentric spatial memory, but also explains why previous excitotoxic lesions have failed to detect any deficits.

[1]  D. Gaffan Scene-Specific Memory for Objects: A Model of Episodic Memory Impairment in Monkeys with Fornix Transection , 1994, Journal of Cognitive Neuroscience.

[2]  Richard S. J. Frackowiak,et al.  Recalling Routes around London: Activation of the Right Hippocampus in Taxi Drivers , 1997, The Journal of Neuroscience.

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

[4]  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.

[5]  M. Meunier,et al.  Electrolytic but not ibotenic acid lesions of the posterior cingulate cortex produce transitory facilitation of learning in mice , 1988, Behavioural Brain Research.

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

[7]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

[8]  J. Taube Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  N. Takahashi,et al.  Pure Topographical Disorientation Due to Right Posterior Cingulate Lesion , 1999, Cortex.

[10]  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.

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

[12]  J. Taube Place cells recorded in the parasubiculum of freely moving rats , 1995, Hippocampus.

[13]  R. Morris,et al.  Spatial learning with a minislab in the dorsal hippocampus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[14]  C. Destrade,et al.  Is a retrosplenial (cingulate) pathway involved in the mediation of high frequency hippocampal rhythmical slow activity (theta)? , 1982, Brain Research.

[15]  E Valenstein,et al.  Retrosplenial amnesia. , 1987, Brain : a journal of neurology.

[16]  Takashi Kawashima,et al.  Mode of [14C] 2-deoxy-d-glucose uptake into retrosplenial cortex and other memory-related structures of the monkey during a delayed response , 1989, Brain Research Bulletin.

[17]  Michael W. Miller,et al.  Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices , 1983, The Journal of comparative neurology.

[18]  S. Mizumori,et al.  Temporary Inactivation of the Retrosplenial Cortex Causes a Transient Reorganization of Spatial Coding in the Hippocampus , 2001, The Journal of Neuroscience.

[19]  A. Elithorn A PRELIMINARY REPORT ON A PERCEPTUAL MAZE TEST SENSITIVE TO BRAIN DAMAGE , 1955, Journal of neurology, neurosurgery, and psychiatry.

[20]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[21]  Amanda Parker,et al.  The effect of anterior thalamic and cingulate cortex lesions on object-in-place memory in monkeys , 1997, Neuropsychologia.

[22]  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.

[23]  E. Maguire The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. , 2001, Scandinavian journal of psychology.

[24]  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.

[25]  E K Warrington,et al.  Selective impairment of memory and visual perception in splenial tumours. , 1991, Brain : a journal of neurology.

[26]  John P Aggleton,et al.  Differential deficits in the Morris water maze following cytotoxic lesions of the anterior thalamus and fornix transection , 1998, Behavioural Brain Research.

[27]  R. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

[28]  R. C. Honey,et al.  Loss of the thalamic nuclei for "head direction" impairs performance on spatial memory tasks in rats. , 2001, Behavioral neuroscience.

[29]  M Gangitano,et al.  Transient topographical amnesia and cingulate cortex damage: A case report , 1996, Neuropsychologia.

[30]  M. W. Brown,et al.  Fos expression in the rostral thalamic nuclei and associated cortical regions in response to different spatial memory tests , 2000, Neuroscience.

[31]  Neil McNaughton,et al.  The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity , 1997, Brain Research.

[32]  Ichiro Akiguchi,et al.  Amnesia following infarction in the right retrosplenial region , 1997, Clinical Neurology and Neurosurgery.

[33]  G. Byatt,et al.  Both anteromedial and anteroventral thalamic lesions impair radial-maze learning in rats. , 1996, Behavioral neuroscience.

[34]  L. Jarrard,et al.  Selective hippocampal lesions and behavior: effects of kainic acid lesions on performance of place and cue tasks. , 1983, Behavioral neuroscience.

[35]  Anna Maria Di Betta,et al.  Retrograde amnesia in a patient with retrosplenial tumour , 1998 .

[36]  Ian Q Whishaw,et al.  Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions , 2001, Behavioural Brain Research.

[37]  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.

[38]  P. Faglioni,et al.  Topographical amnesia. , 1977, Journal of neurology, neurosurgery, and psychiatry.

[39]  Mieke Verfaellie,et al.  Impaired acquisition of temporal information in retrosplenial amnesia , 1988, Brain and Cognition.

[40]  J. Aggleton,et al.  Identifying cortical inputs to the rat hippocampus that subserve allocentric spatial processes: A simple problem with a complex answer , 2000, Hippocampus.

[41]  D. Olton,et al.  Animal Behavior Processes , 2022 .

[42]  F. Gage,et al.  Hippocampal connections and spatial discrimination , 1978, Brain Research.

[43]  H. Shibata,et al.  Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat , 1993, The Journal of comparative neurology.

[44]  S. Mizumori,et al.  Retrosplenial cortex inactivation selectively impairs navigation in darkness. , 1999, Neuroreport.

[45]  D. S. Olton,et al.  A comparative analysis of the role of fornix and cingulate cortex in memory: rats , 2004, Experimental Brain Research.

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

[47]  M. Meunier,et al.  Effects of radiofrequency versus neurotoxic cingulate lesions on spatial reversal learning in mice , 1997, Hippocampus.

[48]  B. McNaughton,et al.  Replay of Neuronal Firing Sequences in Rat Hippocampus During Sleep Following Spatial Experience , 1996, Science.

[49]  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.

[50]  N. Takahashi,et al.  Pure topographic disorientation due to right retrosplenial lesion , 1997, Neurology.

[51]  J. Aggleton,et al.  The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat , 1996, Behavioural Brain Research.

[52]  H. Shibata,et al.  Organization of projections of rat retrosplenial cortex to the anterior thalamic nuclei , 1998, The European journal of neuroscience.