Medial prefrontal cortex is involved in spatial temporal order memory but not spatial recognition memory in tests relying on spontaneous exploration in rats

The present study describes two novel tasks relying on spontaneous patterns of exploration in a radial-arm maze that can be used to assess spatial recognition memory and spatial temporal order memory (i.e. memory for the order in which places have been visited) in the rat. In the recognition memory task, rats were permitted to freely explore two arms in the maze on a first trial and one 'familiar' arm and one novelly located arm on a second trial 105 min later. In the temporal order memory task, rats were permitted to explore two arms in the maze on a first trial, two novel arms on a second trial 60 min later, and one 'older familiar' arm and one 'more recent familiar' arm on a third trial 45 min later. Using these tasks, we found that rats direct greater exploration at a novel than a familiar arm location, thus showing long-term spatial recognition memory, and at an older familiar arm than a more recent familiar arm, thus showing long-term spatial temporal order memory. Lidocaine inactivation of the mPFC prior to the final trial in each task disrupted performance on the temporal order but not the recognition memory task, thereby demonstrating a role for the mPFC in the retrieval and/or use of temporal order information but not in spatial memory per se. These findings highlight the specific involvement of the rat mPFC in temporal order memory and have important implications for a broader understanding of mPFC function.

[1]  N. White,et al.  Dorsal hippocampal function in unreinforced spatial learning , 2000, Hippocampus.

[2]  Bryan Kolb,et al.  Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat , 1982, Neuroscience Letters.

[3]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[4]  R. Passingham The frontal lobes and voluntary action , 1993 .

[5]  M. W. Jones A comparative review of rodent prefrontal cortex and working memory. , 2002, Current molecular medicine.

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

[7]  R. Joosten,et al.  Place and Response Learning of Rats in a Morris Water Maze: Differential Effects of Fimbria Fornix and Medial Prefrontal Cortex Lesions , 2001, Neurobiology of Learning and Memory.

[8]  John B. Mitchell,et al.  The medial frontal cortex and temporal memory: tests using spontaneous exploratory behaviour in the rat , 1998, Behavioural Brain Research.

[9]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[10]  B. Milner,et al.  Frontal lobes and the temporal organization of memory. , 1985, Human neurobiology.

[11]  J. Delacour,et al.  A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data , 1988, Behavioural Brain Research.

[12]  M. Egan,et al.  Memory for temporal order in patients with schizophrenia , 2000, Schizophrenia Research.

[13]  Paul E. Gilbert,et al.  Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1 , 2001, Hippocampus.

[14]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[15]  A. Phillips,et al.  Interaction between Perirhinal and Medial Prefrontal Cortex Is Required for Temporal Order But Not Recognition Memory for Objects in Rats , 2004, The Journal of Neuroscience.

[16]  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.

[17]  D. Joel,et al.  Effects of electrolytic lesions of the medial prefrontal cortex or its subfields on 4-arm baited, 8-arm radial maze, two-way active avoidance and conditioned fear tasks in the rat , 1997, Brain Research.

[18]  D. Warden,et al.  Memory for temporal order in Schizophrenia , 1991, Biological Psychiatry.

[19]  R. Kesner Subregional analysis of mnemonic functions of the prefrontal cortex in the rat , 2000, Psychobiology.

[20]  R P Kesner New approaches to the study of comparative cognition. , 1990, NIDA research monograph.

[21]  Brenda Milner,et al.  The frontal cortex and memory for temporal order , 1991, Neuropsychologia.

[22]  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.

[23]  J. Feldon,et al.  Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory , 2002, Behavioural Brain Research.

[24]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[25]  J. Glowinski,et al.  Hippocampo‐prefrontal cortex pathway: Anatomical and electrophysiological characteristics , 2000, Hippocampus.

[26]  Arthur P. Shimamura,et al.  Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients , 1990, Neuropsychologia.

[27]  M. Petrides,et al.  Specialized systems for the processing of mnemonic information within the primate frontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[28]  Gabriel Leonard,et al.  Frontal-lobe contribution to recency judgements , 1991, Neuropsychologia.

[29]  D. Hannequin,et al.  The Neurobiological Basis of Time Estimation and Temporal Order , 1999, Reviews in the neurosciences.

[30]  Lars Nyberg,et al.  Brain Regions Differentially Involved in Remembering What and When: a PET Study , 1997, Neuron.

[31]  P. Gisquet-Verrier,et al.  Functional role of rat prelimbic-infralimbic cortices in spatial memory: evidence for their involvement in attention and behavioural flexibility , 2000, Behavioural Brain Research.

[32]  T. Robbins,et al.  The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. , 2002, Cerebral cortex.

[33]  R. Sutherland,et al.  A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. , 1983, Behavioral neuroscience.

[34]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[35]  P. Rompré,et al.  Spatial strategy elaboration in egocentric and allocentric tasks following medial prefrontal cortex lesions in the rat , 2001, Brain and Cognition.

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

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

[38]  P. Goldman-Rakic Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. , 1990, Progress in brain research.

[39]  C. Gerfen,et al.  The frontal cortex-basal ganglia system in primates. , 1996, Critical reviews in neurobiology.

[40]  D. Olton,et al.  Cognitive mapping in rats: The role of the hippocampal and frontal systems in retention and reversal , 1981, Behavioural Brain Research.

[41]  Bruno Poucet,et al.  Involvement of the rat prefrontal cortex in cognitive functions: A central role for the prelimbic area , 2000, Psychobiology.

[42]  B. Poucet Object exploration, habituation, and response to a spatial change in rats following septal or medial frontal cortical damage. , 1989, Behavioral neuroscience.

[43]  R. Mair,et al.  The effects of frontal cortical lesions on remembering depend on the procedural demands of tasks performed in the radial arm maze , 1997, Behavioural Brain Research.

[44]  M. Petrides Functional specialization within the dorsolateral frontal cortex for serial order memory , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[46]  E. Tulving,et al.  Memory and Verbal Learning , 1970 .

[47]  J. Aggleton,et al.  Evidence for the Independence of Recognition and Recency Memory in Amnesic Subjects , 1995, Cortex.

[48]  H. Maaswinkel,et al.  Effects of an electrolytic lesion of the prelimbic area on anxiety-related and cognitive tasks in the rat , 1996, Behavioural Brain Research.

[49]  F. Huppert,et al.  Dissociation between learning and remembering in organic amnesia , 1978, Nature.

[50]  Inah Lee,et al.  Time-Dependent Relationship between the Dorsal Hippocampus and the Prefrontal Cortex in Spatial Memory , 2003, The Journal of Neuroscience.

[51]  R. Kesner,et al.  Involvement of the Prelimbic–Infralimbic Areas of the Rodent Prefrontal Cortex in Behavioral Flexibility for Place and Response Learning , 1999, The Journal of Neuroscience.

[52]  Marc A Sommer,et al.  Effective spread and timecourse of neural inactivation caused by lidocaine injection in monkey cerebral cortex , 1997, Journal of Neuroscience Methods.

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

[54]  D. Bilkey,et al.  Prefrontal cortex lesions modify the spatial properties of hippocampal place cells. , 2003, Cerebral cortex.

[55]  W. N. Dember,et al.  Spontaneous alteration after free and forced trials. , 1959, Canadian journal of psychology.

[56]  Raymond P. Kesner,et al.  Serial-position curves in rats: Order memory for episodic spatial events , 1984 .

[57]  L. Cooper,et al.  Memory for temporal order of new and familiar spatial location sequences: role of the medial prefrontal cortex. , 1997, Learning & memory.

[58]  R P Kesner,et al.  Memory for frequency in rats: role of the hippocampus and medial prefrontal cortex. , 1990, Behavioral and neural biology.

[59]  R. O. Hopkins,et al.  Item and Order Recognition Memory in Subjects with Hypoxic Brain Injury , 1995, Brain and Cognition.

[60]  Lars Nyberg,et al.  Age-Related Differences in Neural Activity during Item and Temporal-Order Memory Retrieval: A Positron Emission Tomography Study , 2000, Journal of Cognitive Neuroscience.

[61]  Raymond P. Kesner,et al.  Item and order dissociation in humans with prefrontal cortex damage , 1994, Neuropsychologia.

[62]  Raymond P. Kesner,et al.  Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions , 1987, Neuropsychologia.

[63]  T. Jay,et al.  Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris‐leucoagglutinin , 1991, The Journal of comparative neurology.

[64]  G. N. Brito,et al.  Septohippocampal system and the prelimbic sector of frontal cortex: A neuropsychological battery analysis in the rat , 1990, Behavioural Brain Research.

[65]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[66]  B. Moghaddam,et al.  Distinct contributions of glutamate and dopamine receptors to temporal aspects of rodent working memory using a clinically relevant task , 2001, Psychopharmacology.

[67]  B Poucet,et al.  Medial prefrontal lesions in the rat and spatial navigation: evidence for impaired planning. , 1995, Behavioral neuroscience.

[68]  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.

[69]  Michael D. Kopelman,et al.  Remote and autobiographical memory, temporal context memory and frontal atrophy in Korsakoff and Alzheimer patients , 1989, Neuropsychologia.

[70]  M. E. Corcoran,et al.  Dorsal Hippocampal Kindling Produces a Selective and Enduring Disruption of Hippocampally Mediated Behavior , 2001, The Journal of Neuroscience.

[71]  Patterns of content, contextual, and working memory impairments in schizophrenia and nonamnesic alcoholism. , 1997 .

[72]  R. Kesner,et al.  Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. , 1996, Cerebral cortex.

[73]  Shintaro Funahashi,et al.  Information Processes in the Primate Prefrontal Cortex in Relation to Working Memory Processes , 2002, Reviews in the neurosciences.

[74]  Shintaro Funahashi,et al.  Neuronal mechanisms of executive control by the prefrontal cortex , 2001, Neuroscience Research.

[75]  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.

[76]  D. Olton,et al.  Neuroanatomical bases of spatial memory , 1980, Brain Research.

[77]  M. Van der Linden,et al.  Patients with Schizophrenia Remember that an Event has Occurred, but not When , 1996, British Journal of Psychiatry.

[78]  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.

[79]  B. Milner,et al.  Interhemispheric differences in the localization of psychological processes in man. , 1971, British medical bulletin.

[80]  Takashi Tsukiura,et al.  Neural Basis of Temporal Context Memory: A Functional MRI Study , 2001, NeuroImage.

[81]  R P Kesner,et al.  Involvement of rodent prefrontal cortex subregions in strategy switching. , 1999, Behavioral neuroscience.

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

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

[84]  D. Albert,et al.  Septal hyperreactivity: A comparison of lesions within and adjacent to the septum , 1975, Physiology & Behavior.

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

[86]  P. Lewinsohn,et al.  Short-term memory: a comparison between frontal and nonfrontal right- and left-hemisphere brain-damaged patients. , 1972, Journal of comparative and physiological psychology.

[87]  Bruno Poucet,et al.  Searching for spatial unit firing in the prelimbic area of the rat medial prefrontal cortex , 1997, Behavioural Brain Research.

[88]  D. L. Hintzman Context matching and judgments of recency , 2002, Psychonomic bulletin & review.

[89]  R P Kesner,et al.  Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. , 1994, Behavioral and neural biology.

[90]  Robert Lalonde,et al.  The neurobiological basis of spontaneous alternation , 2002, Neuroscience & Biobehavioral Reviews.

[91]  B. McNaughton,et al.  Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. , 1998, Cerebral cortex.

[92]  C. H. Vanderwolf,et al.  Role of the neocortex in the water maze task in the rat: a detailed behavioral and Golgi-Cox analysis , 2003, Behavioural Brain Research.

[93]  Raymond P. Kesner,et al.  The role of the hippocampus in memory for the temporal order of a sequence of odors. , 2002 .

[94]  S. Funahashi,et al.  Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation , 1997, Behavioural Brain Research.

[95]  Raymond P. Kesner,et al.  Double dissociation of egocentric and allocentric space following medial prefrontal and parietal cortex lesions in the rat. , 1989 .

[96]  P. Rompré,et al.  Involvement of the Medial Prefrontal Cortex in Two Alternation Tasks Using Different Environments , 2002, Brain and Cognition.

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

[98]  A. Ennaceur,et al.  A new one-trial test for neurobiological studies of memory in rats. III. Spatial vs. non-spatial working memory , 1992, Behavioural Brain Research.

[99]  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.

[100]  J. D. Bruin,et al.  A behavioural analysis of rats with damage to the medial prefrontal cortex using the morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation , 1994, Brain Research.

[101]  Bruno Poucet,et al.  Effortful information processing in a spontaneous spatial situation by rats with medial prefrontal lesions , 1996, Behavioural Brain Research.

[102]  Bryan Kolb,et al.  Functions of the frontal cortex of the rat: A comparative review , 1984, Brain Research Reviews.

[103]  N. Stanhope,et al.  Temporal and spatial context memory in patients with focal frontal, temporal lobe, and diencephalic lesions , 1997, Neuropsychologia.

[104]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

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

[106]  J. Tanji,et al.  Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. , 2003, Journal of neurophysiology.