Time Context of Cue-Outcome Associations Represented by Neurons in Perirhinal Cortex

The perirhinal cortex (PRh), which has extensive connections with diverse brain sites, may contribute to semantic memory by associating various types of information about objects. However, the extent of the types of associations in which PRh participates is unknown. In the present study, we let monkeys experience a consistent contingency between visual cues and different types of outcomes (water reward and sound-only acknowledgment) in a particular time context for many days and then recorded neuronal activities from PRh and area TE, which is the major source of visual inputs to PRh. We found that PRh cells represented the outcome type in their responses to the visual cues only in the time context in which the monkeys had experienced the cue-outcome contingency. In contrast, TE cells represented the outcome information whenever the cue appeared (i.e., independently from the related time context). These results showed that PRh cells represented not only the cue-outcome contingency but also the time context in which the monkeys had experienced the contingency. We conclude that PRh is not specific to the representation of sensory and associative properties of objects themselves but may represent broader information about objects, including the time context in which the objects are associated with particular outcomes.

[1]  Yuji Naya,et al.  The perirhinal cortex. , 2014, Annual review of neuroscience.

[2]  Keiji Tanaka,et al.  Cognitive Control Functions of Anterior Cingulate Cortex in Macaque Monkeys Performing a Wisconsin Card Sorting Test Analog , 2014, The Journal of Neuroscience.

[3]  H. Eichenbaum Memory on time , 2013, Trends in Cognitive Sciences.

[4]  M. Shidara,et al.  Stimulus-Related Activity during Conditional Associations in Monkey Perirhinal Cortex Neurons Depends on Upcoming Reward Outcome , 2012, Journal of Neuroscience.

[5]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

[6]  Eric Halgren,et al.  First-Pass Selectivity for Semantic Categories in Human Anteroventral Temporal Lobe , 2011, The Journal of Neuroscience.

[7]  Matthew L Shapiro,et al.  Memory Time , 2011, Neuron.

[8]  Y. Naya,et al.  Integrating What and When Across the Primate Medial Temporal Lobe , 2011, Science.

[9]  Jun Tanji,et al.  Development of Multidimensional Representations of Task Phases in the Lateral Prefrontal Cortex , 2011, The Journal of Neuroscience.

[10]  R. Knight,et al.  The Medial Temporal Lobe Supports Conceptual Implicit Memory , 2010, Neuron.

[11]  O. Pascalis,et al.  Change in background context disrupts performance on visual paired comparison following hippocampal damage , 2009, Neuropsychologia.

[12]  C. Price,et al.  Integrating Visual and Tactile Information in the Perirhinal Cortex , 2009, Cerebral cortex.

[13]  E. Procyk,et al.  Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex , 2008, Neuron.

[14]  J. Tanji,et al.  Role of the lateral prefrontal cortex in executive behavioral control. , 2008, Physiological reviews.

[15]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[16]  Keiji Tanaka,et al.  Medial prefrontal cell activity signaling prediction errors of action values , 2007, Nature Neuroscience.

[17]  L. Davachi Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

[18]  Keiji Tanaka,et al.  Reward Association Affects Neuronal Responses to Visual Stimuli in Macaque TE and Perirhinal Cortices , 2006, The Journal of Neuroscience.

[19]  L. Tyler,et al.  Binding crossmodal object features in perirhinal cortex. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  K. Saleem,et al.  Differential connections of the perirhinal and parahippocampal cortex with the orbital and medial prefrontal networks in macaque monkeys , 2005, The Journal of comparative neurology.

[21]  Keiji Tanaka,et al.  Prior experience of rotation is not required for recognizing objects seen from different angles , 2005, Nature Neuroscience.

[22]  Guy B. Williams,et al.  The human perirhinal cortex and semantic memory , 2004, The European journal of neuroscience.

[23]  Richard C Saunders,et al.  DNA targeting of rhinal cortex D2 receptor protein reversibly blocks learning of cues that predict reward. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Wise Dopamine, learning and motivation , 2004, Nature Reviews Neuroscience.

[25]  James L. McClelland,et al.  The parallel distributed processing approach to semantic cognition , 2003, Nature Reviews Neuroscience.

[26]  L. Squire,et al.  Neuronal representations of stimulus associations develop in the temporal lobe during learning , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  E. Murray,et al.  Neural substrates of crossmodal association memory in monkeys: the amygdala versus the anterior rhinal cortex. , 2001, Behavioral neuroscience.

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

[29]  B. Richmond,et al.  Learning motivational significance of visual cues for reward schedules requires rhinal cortex , 2000, Nature Neuroscience.

[30]  B. Richmond,et al.  Response differences in monkey TE and perirhinal cortex: stimulus association related to reward schedules. , 2000, Journal of neurophysiology.

[31]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[32]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

[33]  D. Gaffan,et al.  Lesions of the primate rhinal cortex cause deficits in flavour–visual associative memory , 1998, Behavioural Brain Research.

[34]  D. Gaffan,et al.  Perirhinal cortex ablation impairs configural learning and paired–associate learning equally , 1998, Neuropsychologia.

[35]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[36]  D. Amaral,et al.  Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys , 1996, The Journal of comparative neurology.

[37]  Keiji Tanaka,et al.  Representation of Visual Features of Objects in the Inferotemporal Cortex , 1996, Neural Networks.

[38]  K. Tanaka,et al.  Divergent Projections from the Anterior Inferotemporal Area TE to the Perirhinal and Entorhinal Cortices in the Macaque Monkey , 1996, The Journal of Neuroscience.

[39]  J. Joyce,et al.  Dopamine D2 receptors are organized in bands in normal human temporal cortex , 1996, Neuroscience.

[40]  Y. Miyashita,et al.  Formation of mnemonic neuronal responses to visual paired associates in inferotemporal cortex is impaired by perirhinal and entorhinal lesions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[42]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[43]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TE and TEO with medial temporal- lobe structures in infant and adult monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[45]  L. J. Hammond The effect of contingency upon the appetitive conditioning of free-operant behavior. , 1980, Journal of the experimental analysis of behavior.