Involvement of the rat prefrontal cortex in cognitive functions: A central role for the prelimbic area

In this brief review, we address the cognitive functions of a subregion of the rat frontal cortex, the prelimbic cortex. Growing evidence suggests that the prelimbic cortex is involved in working memory, defined as the temporary storage of information required for its internal manipulation. However, several factors appear to modulate the extent to which prelimbic damage impairs performance in delayed tasks. These factors, which contribute to the overall difficulty of the task, are related to the attentional requirement of the task and to the response selection mechanisms that underlie correct performance. Impairments induced by prelimbic cortical damage are increased when the task requires the rat to consistently focus its attention on the detection of external events and when the learning rule countradicts either spontaneously used or previously learned strategies. This overall pattern of deficit suggests that the prelimbic cortex is not a pure working memory system. Rather, it subtends a wide range of processes that are required for solving difficult problems. Together with anatomical evidence, the existence of functional similarities between the prelimbic cortex of the rat and the dorsolateral prefrontal cortex of primates suggests some homology between these regions across species. Therefore, the rat prelimbic cortex appears to provide a valuable model system for studying the precursors of higher level cognitive processes in nonhuman and human primates.

[1]  T. Robbins,et al.  Neural Systems Underlying Arousal and Attention: Implications for Drug Abuse a , 1998, Annals of the New York Academy of Sciences.

[2]  Prof. Dr. Karl Zilles The Cortex of the Rat , 1985, Springer Berlin Heidelberg.

[3]  Bruno Poucet,et al.  Evidence for the Involvement of the Rat Prefrontal Cortex in Sustained Attention , 1998, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[4]  B Poucet,et al.  Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. , 1994, Behavioral neuroscience.

[5]  J. M. Warren,et al.  THE FRONTAL GRANULAR CORTEX AND BEHAVIOR , 1964 .

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

[7]  I. Divac,et al.  Selective ablations within the prefrontal cortex of the rat and performance of delayed alternation , 1978 .

[8]  J. Fuster The Prefrontal Cortex , 1997 .

[9]  B. Kolb,et al.  The Cerebral cortex of the rat , 1990 .

[10]  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.

[11]  M. Corbetta,et al.  Imaging studies of memory and attention. , 1997, Neurosurgery clinics of North America.

[12]  J. D. Bruin,et al.  Spatial delayed alternation of rats in a T-maze: effects of neurotoxic lesions of the medial prefrontal cortex and of T-maze rotations , 1997, Behavioural Brain Research.

[13]  John A. Harvey,et al.  COCAINE: EFFECTS ON THE DEVELOPING BRAIN , 1998 .

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

[15]  T. Robbins,et al.  Dissociation in prefrontal cortex of affective and attentional shifts , 1996, Nature.

[16]  T. Shallice,et al.  A Multidisciplinary Approach to Anterior Attentional Functions a , 1995, Annals of the New York Academy of Sciences.

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

[19]  A. Kertesz Localization in neuropsychology , 1983 .

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

[21]  Keith J. Holyoak,et al.  Structure and Functions of the Human Prefrontal Cortex , 1996 .

[22]  W. Schmidt,et al.  Discrete quinolinic acid lesions of the rat prelimbic medial prefrontal cortex affect cocaine- and MK-801-, but not morphine- and amphetamine-induced reward and psychomotor activation as measured with the place preference conditioning paradigm , 1998, Behavioural Brain Research.

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

[24]  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.

[25]  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.

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

[27]  J. Horton,et al.  Medial prefrontal lesion deficits involving or sparing the prelimbic area in the rat , 1998, Physiology & Behavior.

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

[29]  Liang Li,et al.  Restricted lesions to ventral prefrontal subareas block reversal learning but not visual discrimination learning in rats , 1998, Physiology & Behavior.

[30]  T. Preuss Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[31]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[32]  B. Milner Effects of Different Brain Lesions on Card Sorting: The Role of the Frontal Lobes , 1963 .

[33]  J. Muir,et al.  The cerebral cortex of the rat and visual attentional function: dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time task. , 1996, Cerebral cortex.

[34]  M. Posner,et al.  Attentional networks , 1994, Trends in Neurosciences.

[35]  H. Uylings,et al.  Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. , 1990, Progress in brain research.

[36]  Karl J. Zilles,et al.  The Cortex of the Rat: A Stereotaxic Atlas , 1985 .

[37]  N. J. Herrod,et al.  Redefining the functional organization of working memory processes within human lateral prefrontal cortex , 1999, The European journal of neuroscience.

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

[39]  T. Jay,et al.  Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat , 1989, Brain Research.

[40]  Gordon Winocur,et al.  Functional dissociation of the hippocampus and prefrontal cortex in learning and memory , 1991, Psychobiology.

[41]  J. Price,et al.  The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat , 1977, The Journal of comparative neurology.

[42]  N. V. Poll,et al.  Delayed spatial response alternation: Effects of delay-interval duration and lesions of the medial prefrontal cortex on response accuracy of male and female Wistar rats , 1985, Behavioural Brain Research.

[43]  M Moscovitch,et al.  Frontal Lobes, Memory, and Aging , 1995, Annals of the New York Academy of Sciences.

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

[45]  V. Johnston,et al.  The nature of the medial wall deficit in the rat. , 1974, Neuropsychologia.

[46]  R. Church,et al.  Attention and the frontal cortex as examined by simultaneous temporal processing , 1988, Neuropsychologia.

[47]  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.

[48]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

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

[50]  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.

[51]  B. Milner,et al.  Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man , 1982, Neuropsychologia.

[52]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[53]  Alan C. Evans,et al.  Time-Related Changes in Neural Systems Underlying Attention and Arousal During the Performance of an Auditory Vigilance Task , 1997, Journal of Cognitive Neuroscience.

[54]  P. Gisquet-Verrier,et al.  Lesions of the prelimbic-infralimbic cortices in rats do not disrupt response selection processes but induce delay-dependent deficits: evidence for a role in working memory? , 1999, Behavioral neuroscience.

[55]  T. Robbins Arousal systems and attentional processes , 1997, Biological Psychology.

[56]  G. N. Brito,et al.  Recovery of delayed alternation in rats after lesions in medial frontal cortex and septum. , 1980, Journal of comparative and physiological psychology.

[57]  J. D. Brabander,et al.  Comparison of the effects of neonatal and adult medial prefrontal cortex lesions on food hoarding and spatial delayed alternation , 1991, Behavioural Brain Research.

[58]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  Françoise Condé,et al.  Afferent connections of the medial frontal cortex of the rat. A study using retrograde transport of fluorescent dyes. I. Thalamic afferents , 1990, Brain Research Bulletin.

[60]  V. Mountcastle,et al.  Higher functions of the brain , 1987 .

[61]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

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

[63]  Daphna Joel,et al.  Electrolytic lesions of the medial prefrontal cortex in rats disrupt performance on an analog of the Wisconsin Card Sorting Test, but do not disrupt latent inhibition: implications for animal models of schizophrenia , 1997, Behavioural Brain Research.

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

[65]  T. Bussey,et al.  Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. , 1997, Behavioral neuroscience.

[66]  J. Webster,et al.  Frontal Lobe Lesions and Behavior* , 1981, Southern medical journal.

[67]  S B Dunnett,et al.  Role of prefrontal cortex and striatal output systems in short-term memory deficits associated with ageing, basal forebrain lesions, and cholinergic-rich grafts. , 1990, Canadian journal of psychology.

[68]  E. Audinat,et al.  Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents , 1995, The Journal of comparative neurology.

[69]  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.

[70]  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.

[71]  H. Groenewegen,et al.  The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. , 1990, Progress in brain research.