Time-Dependent Relationship between the Dorsal Hippocampus and the Prefrontal Cortex in Spatial Memory

The prefrontal cortex and the dorsal hippocampus have been studied extensively for their significant roles in spatial working memory. A possible time-dependent functional relationship between the prefrontal cortex and the dorsal hippocampus in spatial working memory was tested. A combined lesion and pharmacological inactivation technique targeting both the dorsal hippocampus and the medial prefrontal cortex was used (i.e., axon-sparing lesions of the dorsal hippocampus combined with reversible inactivation of the medial prefrontal cortex, or vice versa, within a subject). A delayed nonmatching-to-place task on a radial eight-arm maze with short-term (i.e., 10 sec) versus intermediate-term (i.e., 5 min) delays was used as a behavioral paradigm. Here we report that the dorsal hippocampus and the medial prefrontal cortex process short-term spatial memory in parallel, serving as a compensatory mechanism for each other. The role of the dorsal hippocampus, however, becomes highlighted as the time-window for memory (i.e., delay) shifts from short-term to a delay period (i.e., intermediate-term) exceeding the short-term range. The results indicate that the time window of memory is a key factor in dissociating multiple memory systems.

[1]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[2]  R P Kesner,et al.  Short-term memory for duration and distance in humans: role of the hippocampus. , 2001, Neuropsychology.

[3]  A. David Redish,et al.  The hippocampal debate: are we asking the right questions? , 2001, Behavioural Brain Research.

[4]  Jeansok J Kim,et al.  Multiple brain-memory systems: the whole does not equal the sum of its parts , 2001, Trends in Neurosciences.

[5]  R. Clark,et al.  Rats with lesions of the hippocampus are impaired on the delayed nonmatching‐to‐sample task † , 2001, Hippocampus.

[6]  John H. Martin Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat , 1991, Neuroscience Letters.

[7]  J. Aggleton,et al.  The performance of amnesic subjects on tests of delayed matching-to-sample and delayed matching-to-position , 1995, Neuropsychologia.

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

[9]  Lynn Nadel,et al.  Multiple Memory Systems: What and Why , 1992, Journal of Cognitive Neuroscience.

[10]  M. Mishkin,et al.  The anatomy of memory. , 1987, Scientific American.

[11]  R. Dias,et al.  Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching‐ and matching‐to‐place in the T‐maze in the rat: differential involvement of the prelimbic–infralimbic and anterior cingulate cortices in providing behavioural flexibility , 2000, The European journal of neuroscience.

[12]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

[13]  R. Kesner,et al.  Equivalent spatial location memory deficits in rats with medial septum or hippocampal formation lesions and patients with dementia of the Alzheimer's type , 1989, Brain and Cognition.

[14]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[15]  P. Andersen,et al.  Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  R. Kesner Retrospective and prospective coding of information: role of the medial prefrontal cortex , 2004, Experimental Brain Research.

[17]  E. Rolls,et al.  Role of long‐term synaptic modification in short‐term memory , 2001, Hippocampus.

[18]  A. Parkin Human memory: Novelty, association and the brain , 1997, Current Biology.

[19]  R. Kesner,et al.  The Effects of Prelimbic and Infralimbic Lesions on Working Memory for Visual Objects in Rats , 2002, Neurobiology of Learning and Memory.

[20]  P. Gisquet-Verrier,et al.  Prelimbic cortex specific lesions disrupt delayed-variable response tasks in the rat. , 1996, Behavioral neuroscience.

[21]  J. Aggleton,et al.  The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats , 1993, Behavioural Brain Research.

[22]  J. Seamans,et al.  Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay , 1997, The Journal of Neuroscience.

[23]  E. Miller,et al.  THE PREFRONTAL CORTEX AND COGNITIVE CONTROL , 2000 .

[24]  Christos Constantinidis,et al.  The sensory nature of mnemonic representation in the primate prefrontal cortex , 2001, Nature Neuroscience.

[25]  J. Tanji,et al.  Behavioral planning in the prefrontal cortex , 2001, Current Opinion in Neurobiology.

[26]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[27]  H. Eichenbaum A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[28]  L. Jarrard On the role of the hippocampus in learning and memory in the rat. , 1993, Behavioral and neural biology.

[29]  Inah Lee,et al.  Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory , 2002, Nature Neuroscience.

[30]  R. Morris,et al.  Delay‐dependent impairment of a matching‐to‐place task with chronic and intrahippocampal infusion of the NMDA‐antagonist D‐AP5 , 1999, Hippocampus.

[31]  G Lynch,et al.  Distinct memory circuits composing the hippocampal region , 1996, Hippocampus.

[32]  L. Nadel,et al.  Multiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results , 2000, Hippocampus.

[33]  Y. Izaki,et al.  Effects of rat medial prefrontal cortex temporal inactivation on a delayed alternation task , 2001, Neuroscience Letters.

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

[35]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[36]  R P Kesner,et al.  Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. , 1998, Behavioral neuroscience.

[37]  Gustavo Deco,et al.  Computational neuroscience of vision , 2002 .

[38]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[39]  Ivan Toni,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[40]  C. Stern,et al.  Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli , 2001, Hippocampus.

[41]  U. Stäubli,et al.  Short‐term reverberant memory model of hippocampal field CA3 , 1997, Hippocampus.

[42]  Jeremy K. Seamans,et al.  Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. , 1995, Behavioral neuroscience.

[43]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.

[44]  R. Hampson,et al.  Effects of Ibotenate Hippocampal and Extrahippocampal Destruction on Delayed-Match and -Nonmatch-to-Sample Behavior in Rats , 1999, The Journal of Neuroscience.

[45]  N. Berthier The role of the extraocular muscles in the rabbit nictitating membrane response: a re-examination , 1984, Behavioural Brain Research.

[46]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[47]  J. M. Novak,et al.  Serial position curve in rats: role of the dorsal hippocampus. , 1982, Science.

[48]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[49]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[50]  R. Mair,et al.  A comparison of the effects of hippocampal or prefrontal cortical lesions on three versions of delayed non-matching-to-sample based on positional or spatial cues , 2000, Behavioural Brain Research.

[51]  P Alvarez,et al.  The animal model of human amnesia: long-term memory impaired and short-term memory intact. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Gordon Winocur,et al.  A comparison of normal old rats and young adult rats with lesions to the hippocampus or prefrontal cortex on a test of matching-to-sample , 1992, Neuropsychologia.