Neural Correlates of Olfactory Recognition Memory in the Rat Orbitofrontal Cortex

The orbitofrontal cortex (OF) is strongly and reciprocally connected with the perirhinal (PR) and entorhinal areas of the medial temporal lobe and plays an important role in odor recognition memory. This study characterized firing patterns of single neurons in the OF of rats performing a continuous odor-guided delayed nonmatch to sample (DNMS) task. Most OF neurons fired in association with one or more task events, including the initiation of trials, the sampling of odor stimuli, and the consumption of rewards. OF neurons also exhibited sustained odor-selective activity during the memory delay, and a large proportion of OF cells had odor-specific enhanced or suppressed responses on stimulus repetition. Most OF neurons were activated during several task events, or associated with complex behavioral states. The incidence of cells that fired in association with the critical match/non-match judgement was increased as the DNMS rule was learned, and was higher in OF than in perirhinal and entorhinal cortex. Furthermore, the classification of match and nonmatch trials was correlated with accuracy in performance of that judgement. These findings are consistent with the view that OF is a high order association cortex that plays a role both in the memory representations for specific stimuli and in the acquisition and application of task rules.

[1]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[2]  R. Desimone,et al.  Scopolamine affects short-term memory but not inferior temporal neurons. , 1993, Neuroreport.

[3]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

[4]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[5]  G. Schoenbaum,et al.  Information coding in the rodent prefrontal cortex. II. Ensemble activity in orbitofrontal cortex. , 1995, Journal of neurophysiology.

[6]  H Eichenbaum,et al.  Afferent connections of the perirhinal cortex in the rat , 1983, The Journal of comparative neurology.

[7]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task , 1992 .

[8]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[9]  E. Miller,et al.  Neural Activity in the Primate Prefrontal Cortex during Associative Learning , 1998, Neuron.

[10]  C G Gross,et al.  Responses of inferior temporal cortex and hippocampal neurons during delayed matching to sample in monkeys (Macaca fascicularis). , 1994, Behavioral neuroscience.

[11]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[13]  J. Fuster,et al.  Mnemonic and predictive functions of cortical neurons in a memory task , 1992, Neuroreport.

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

[15]  J. Fuster.  Memory in the cerebral cortex , 1994 .

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

[17]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[18]  E. Miller,et al.  Prospective Coding for Objects in Primate Prefrontal Cortex , 1999, The Journal of Neuroscience.

[19]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Cohen,et al.  Context, cortex, and dopamine: a connectionist approach to behavior and biology in schizophrenia. , 1992, Psychological review.

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

[22]  H. Eichenbaum,et al.  Memory Representation within the Parahippocampal Region , 1997, The Journal of Neuroscience.

[23]  D. Gaffan,et al.  Recognition impaired and association intact in the memory of monkeys after transection of the fornix. , 1974, Journal of comparative and physiological psychology.

[24]  M. W. Brown.  Neuronal responses and recognition memory , 1996 .

[25]  M Mishkin,et al.  An analysis of short-term visual memory in the monkey. , 1975, Journal of experimental psychology. Animal behavior processes.

[26]  E. Rolls,et al.  Orbitofrontal cortex neurons: role in olfactory and visual association learning. , 1996, Journal of neurophysiology.

[27]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[28]  R. Desimone,et al.  Object and place memory in the macaque entorhinal cortex. , 1997, Journal of neurophysiology.

[29]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[30]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[31]  E. Murray,et al.  Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. , 1992, Behavioral neuroscience.

[32]  J. Price,et al.  Olfactory Input to the Prefrontal Cortex in the Rat , 1987 .

[33]  Larry W. Swanson,et al.  Brain Maps: Structure of the Rat Brain , 1992 .

[34]  H. Eichenbaum,et al.  Neuronal activity in the hippocampus during delayed non‐match to sample performance in rats: Evidence for hippocampal processing in recognition memory , 1992, Hippocampus.

[35]  H. Eichenbaum,et al.  Crossmodal Associative Memory Representations in Rodent Orbitofrontal Cortex , 1999, Neuron.

[36]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[37]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. , 1992, Behavioral neuroscience.

[39]  E. Murray,et al.  Preserved Recognition Memory for Small Sets, and Impaired Stimulus Identification for Large Sets, Following Rhinal Cortex Ablations in Monkeys , 1994, The European journal of neuroscience.

[40]  Seth J. Ramus,et al.  Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system , 1994, Hippocampus.

[41]  Masataka Watanabe.  Reward expectancy in primate prefrental neurons , 1996, Nature.

[42]  D. Mumby,et al.  Rhinal cortex lesions and object recognition in rats. , 1994, Behavioral neuroscience.

[43]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  Seth J. Ramus,et al.  Dissociation between the effects of damage to perirhinal cortex and area TE. , 1999, Learning & memory.

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

[47]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

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

[49]  H. Barbas,et al.  Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey , 1993, Neuroscience.

[50]  H Eichenbaum,et al.  Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. , 1995, Journal of neurophysiology.