Delay activity in avian prefrontal cortex – sample code or reward code?

In the current study, we examined whether delay activity in the avian equivalent of the prefrontal cortex (PFC) represents a neural correlate of a to‐be‐remembered sample stimulus or an upcoming reward. Birds were trained on a directed forgetting paradigm in which sample stimuli (red and white) were either followed by a cue to remember (high‐frequency tone) or a cue to forget (low‐frequency tone). The task also incorporated a differential outcomes procedure in which a correct response on the memory test following a red (remember) sample was rewarded with food, but correct responses on the memory test following the white (remember) sample were not. If delay activity represents a sample code, then it should be seen on both red‐remember and white‐remember trials. On the other hand, if delay activity represents a reward code, then delay activity should be seen only on red‐remember trials, but not white‐remember trials. Our findings suggest that activity in the avian PFC represents the outcome associated with each sample (reward or no reward) rather than memory for the sample itself.

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

[2]  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.

[3]  C. Gross,et al.  Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. , 1998, Journal of neurophysiology.

[4]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  M. Mishkin,et al.  Non-spatial memory after selective prefrontal lesions in monkeys , 1978, Brain Research.

[6]  Joaquin M. Fuster,et al.  Effects of cooling inferotemporal cortex on performance of visual memory tasks , 1981, Experimental Neurology.

[7]  S. Mohand-Said,et al.  Neurodegenerative and Neuroprotective Effects of Tumor Necrosis Factor (TNF) in Retinal Ischemia: Opposite Roles of TNF Receptor 1 and TNF Receptor 2 , 2002, The Journal of Neuroscience.

[8]  E. Save,et al.  Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  P. L. Brown,et al.  Auto-shaping of the pigeon's key-peck. , 1968, Journal of the experimental analysis of behavior.

[10]  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.

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

[12]  O. Güntürkün,et al.  Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): A retro‐ and anterograde pathway tracing study , 1999, The Journal of comparative neurology.

[13]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[14]  Michael Colombo,et al.  A lightweight microdrive for single-unit recording in freely moving rats and pigeons. , 2003, Methods.

[15]  J. A. Horel,et al.  Reversible cold lesions of the parahippocampal gyrus in monkeys result in deficits on the delayed match-to-sample and other visual tasks , 1989, Behavioural Brain Research.

[16]  M. Ungless,et al.  Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli , 2009, Proceedings of the National Academy of Sciences.

[17]  G. Keppel,et al.  Design and Analysis: A Researcher's Handbook , 1976 .

[18]  J. Overmier,et al.  Conditional choice-unique outcomes establish expectancies that mediate choice behavior , 2001, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[19]  Jonas Rose,et al.  Neural Correlates of Executive Control in the Avian Brain , 2005, PLoS biology.

[20]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[21]  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.

[22]  M. R. D’amato Delayed Matching and Short-Term Memory in Monkeys1 , 1973 .

[23]  O. Güntürkün Avian and mammalian “prefrontal cortices”: Limited degrees of freedom in the evolution of the neural mechanisms of goal-state maintenance , 2005, Brain Research Bulletin.

[24]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[25]  O. Güntürkün Cognitive impairments after lesions of the neostriatum caudolaterale and its thalamic afferent in pigeons: functional similarities to the mammalian prefrontal system? , 1997, Journal fur Hirnforschung.

[26]  Onur Güntürkün,et al.  Working Memory Neurons in Pigeons , 2002, The Journal of Neuroscience.

[27]  Ewelina Knapska,et al.  Differential involvement of the central amygdala in appetitive versus aversive learning. , 2006, Learning & memory.

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

[29]  Y. Sakurai,et al.  Multiple unit activity of prefrontal cortex and dorsomedial thalamus during delayed go/no-go alternation in the rat , 1986, Behavioural Brain Research.

[30]  K. Hikosaka,et al.  Delay activity of orbital and lateral prefrontal neurons of the monkey varying with different rewards. , 2000, Cerebral cortex.

[31]  J. Fuster,et al.  Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. , 1981, Science.

[32]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[33]  M. Colombo,et al.  Responses of ectostriatal neurons during delayed matching-to-sample behavior in pigeons (Columba livia) , 2001, Brain Research.

[34]  M. Colombo,et al.  Neural correlates of directed forgetting in the avian prefrontal cortex. , 2008, Behavioral neuroscience.

[35]  T. Zentall,et al.  Directed forgetting in animals. , 1993, Psychological bulletin.

[36]  O. Güntürkün The avian ‘prefrontal cortex’ and cognition , 2005, Current Opinion in Neurobiology.

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

[38]  H. Karten,et al.  A stereotaxic atlas of the brain of the pigeon (Columba livia) , 1967 .