Testing the importance of the retrosplenial navigation system: lesion size but not strain matters: a reply to Harker and Whishaw

In their review on the retrosplenial cortex Harker and Whishaw [Neurosci Biobehav Rev, 2004] claim that there is continued disagreement over the importance of this region for navigation. They argue that discrepancies in the published effects of retrosplenial lesions reflect two principal variables, choice of rat strain and choice of spatial task. In this reply, evidence is provided showing that Harker and Whishaw [Neurosci Biobehav Rev, 2004] have created a misleading impression and, in fact, there is a clear consensus that the rat retrosplenial cortex is necessary for navigation. Likewise, there is no dispute that the effects of retrosplenial lesions will differ for different tests of spatial learning. While Harker and Whishaw [Neurosci Biobehav Rev, 2004] also conclude that choice of rat strain has a critical impact on whether a lesion-induced deficit is found, a comprehensive review of the published data shows no systematic strain difference. There is, however, growing evidence that when interpreting the effects of retrosplenial lesions, account should be given of the lesion method and its interaction with lesion size.

[1]  P. E. Sharp,et al.  Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. , 2001, Behavioral neuroscience.

[2]  John P. Aggleton,et al.  Testing the importance of the retrosplenial guidance system: effects of different sized retrosplenial cortex lesions on heading direction and spatial working memory , 2004, Behavioural Brain Research.

[3]  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.

[4]  R. Douglas.  Cues for spontaneous alternation. , 1966, Journal of comparative and physiological psychology.

[5]  W. Low,et al.  Intraretrosplenial cortical grafts of fetal cholinergic neurons and the restoration of spatial memory function. , 1997, Cell transplantation.

[6]  M. F. Brown,et al.  Does a cognitive map guide choices in the radial-arm maze? , 1992, Journal of experimental psychology. Animal behavior processes.

[7]  Seralynne D Vann,et al.  Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. , 2002, Behavioral neuroscience.

[8]  J. Muir,et al.  A behavioural analysis of the delayed non-matching to position task: the effects of scopolamine, lesions of the fornix and of the prelimbic region on mediating behaviours by rats , 1997, Psychopharmacology.

[9]  I. Whishaw,et al.  Place and matching-to-place spatial learning affected by rat inbreeding (Dark–Agouti, Fischer 344) and albinism (Wistar, Sprague–Dawley) but not domestication (wild rat vs. Long–Evans, Fischer–Norway) , 2002, Behavioural Brain Research.

[10]  W. N. Dember,et al.  Spontaneous alternation behavior. , 1958, Psychological bulletin.

[11]  F. Restle.  Discrimination of cues in mazes: a resolution of the place-vs.-response question. , 1957, Psychological review.

[12]  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.

[13]  I. Whishaw,et al.  Variation in visual acuity within pigmented, and between pigmented and albino rat strains , 2002, Behavioural Brain Research.

[14]  W. N. Dember,et al.  Spontaneous alternation behavior. , 1958, Psychological bulletin.

[15]  Ian Q. Whishaw,et al.  A reaffirmation of the retrosplenial contribution to rodent navigation: reviewing the influences of lesion, strain, and task , 2004, Neuroscience & Biobehavioral Reviews.

[16]  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.

[17]  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.

[18]  T. Alexinsky.  Differential effect of thalamic and cortical lesions on memory systems in the rat , 2001, Behavioural Brain Research.

[19]  A. Black,et al.  Stimulus control of spatial behavior on the eight-arm maze in rats ☆ ☆☆ , 1980 .

[20]  P. Dudchenko,et al.  How do animals actually solve the T maze? , 2001, Behavioral neuroscience.

[21]  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.

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

[23]  A. Young,et al.  A comparison between Dark Agouti and Sprague-Dawley rats in their behaviour on the elevated plus-maze, open-field apparatus and activity meters, and their response to diazepam , 2002, Psychopharmacology.

[24]  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.

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

[26]  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.

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

[28]  C. Dourish,et al.  Dissociation between cognitive and motor/motivational deficits in the delayed matching to position test: effects of scopolamine, 8-OH-DPAT and EAA antagonists , 1995, Psychopharmacology.

[29]  M. F. Brown,et al.  Erratum to: In the dark II: Spatial choice when access to extrinsic spatial cues is eliminated , 1997 .

[30]  I. Whishaw,et al.  Impaired Spatial Performance in Rats with Retrosplenial Lesions: Importance of the Spatial Problem and the Rat Strain in Identifying Lesion Effects in a Swimming Pool , 2002, The Journal of Neuroscience.

[31]  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.

[32]  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.

[33]  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.

[34]  Seralynne D Vann,et al.  Testing the importance of the caudal retrosplenial cortex for spatial memory in rats , 2003, Behavioural Brain Research.

[35]  I. Whishaw,et al.  Impaired place navigation in place and matching‐to‐place swimming pool tasks follows both retrosplenial cortex lesions and cingulum bundle lesions in rats , 2004, Hippocampus.

[36]  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.