Activity of Primate Orbitofrontal and Dorsolateral Prefrontal Neurons: Effect of Reward Schedule on Task-related Activity

Recent studies show that task-related activity in the dorsolateral prefrontal cortex (DLPFC) is modulated by the quality and quantity of the reward, suggesting that the subject's motivational state affects cognitive operations in the DLPFC. The orbito-frontal cortex (OFC) is a possible source of motivational inputs to the DLPFC. However, it is not well known whether these two areas exhibit similar motivational effects on task-related activity. We compared motivational effects on task-related activity in these areas while a monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, reward was given only after the successful completion of four consecutive trials, whereas in the ODR-2 schedule, reward was given after every correct trial. Task-related activities in both areas showed spatial selectivity. The spatial characteristics of task-related activity remained constant in both schedules. Task-related activity in both areas, especially delay-period activity, was also affected by the reward schedule and the magnitude of the activity gradually increased depending on the proximity of the reward trial in the ODR-1 schedule. More task-related OFC activities were affected by reward schedules, whereas more task-related DLPFC activities were affected by spatial factors and reward schedules. These results indicate that the OFC plays a role in monitoring the proximity of the reward trial and detecting reward delivery, whereas the DLPFC plays a role in performing cognitive operations and integrating cognitive and motivational information. These results also indicate that spatial information and the animal's motivational state independently affect neuronal activity in both areas.

[1]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[2]  M. Roesch,et al.  Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex , 2004, Science.

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

[4]  O. Hikosaka,et al.  Influence of reward expectation on visuospatial processing in macaque lateral prefrontal cortex. , 2002, Journal of neurophysiology.

[5]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[6]  B. Kushner Descartes' error. , 1998, Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus.

[7]  Shintaro Funahashi,et al.  Reward-period Activity in Primate Dorsolateral Prefrontal and Orbitofrontal Neurons Is Affected by Reward Schedules , 2006, Journal of Cognitive Neuroscience.

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

[9]  E. Rolls,et al.  Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. , 1996, Journal of neurophysiology.

[10]  D. Stuss,et al.  The Frontal Lobes , 1986 .

[11]  Masataka Watanabe,et al.  Long‐ and short‐range reward expectancy in the primate orbitofrontal cortex , 2004, The European journal of neuroscience.

[12]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

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

[14]  M. Shadlen,et al.  Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque , 1999, Neuron.

[15]  P. Goldman-Rakic,et al.  Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. , 1991, Journal of neurophysiology.

[16]  M. Roesch,et al.  Neuronal activity in primate orbitofrontal cortex reflects the value of time. , 2005, Journal of neurophysiology.

[17]  Shintaro Funahashi,et al.  Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks. , 2002, Journal of neurophysiology.

[18]  W. Schultz,et al.  Reward-related neuronal activity during go-nogo task performance in primate orbitofrontal cortex. , 2000, Journal of neurophysiology.

[19]  Akira Murata,et al.  Ipsilateral connections of the anterior cingulate cortex with the frontal and medial temporal cortices in the macaque monkey , 1994, Neurosciences research.

[20]  M. Roesch,et al.  Neuronal activity dependent on anticipated and elapsed delay in macaque prefrontal cortex, frontal and supplementary eye fields, and premotor cortex. , 2005, Journal of neurophysiology.

[21]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[22]  Joaquin M. Fuster,et al.  Single cell activity in ventral prefrontal cortex of behaving monkeys , 1981, Brain Research.

[23]  S. Funahashi,et al.  Activity of primate orbitofrontal and dorsolateral prefrontal neurons: task-related activity during an oculomotor delayed-response task , 2007, Experimental Brain Research.

[24]  B. Richmond,et al.  Neuronal Signals in the Monkey Ventral Striatum Related to Progress through a Predictable Series of Trials , 1998, The Journal of Neuroscience.

[25]  F. Plum Handbook of Physiology. , 1960 .

[26]  J. Joseph,et al.  Prefrontal unit activity during a delayed oculomotor task in the monkey , 2004, Experimental Brain Research.

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

[28]  C. Cavada,et al.  The anatomical connections of the macaque monkey orbitofrontal cortex. A review. , 2000, Cerebral cortex.

[29]  Joaquín M. Fuster,et al.  Cortex and Memory: Emergence of a New Paradigm , 2009, Journal of Cognitive Neuroscience.

[30]  Jonathan D. Wallis,et al.  Neurons in the Frontal Lobe Encode the Value of Multiple Decision Variables , 2009, Journal of Cognitive Neuroscience.

[31]  B. Richmond,et al.  Anterior Cingulate: Single Neuronal Signals Related to Degree of Reward Expectancy , 2002, Science.

[32]  Shintaro Funahashi,et al.  Reward acts as a signal to control delay-period activity in delayed-response tasks , 2010, Neuroreport.

[33]  K. Hikosaka,et al.  Coding and Monitoring of Motivational Context in the Primate Prefrontal Cortex , 2002, The Journal of Neuroscience.

[34]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[35]  J. Fuster Prefrontal Cortex , 2018 .

[36]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[37]  B. Richmond,et al.  Neural signals in the monkey ventral striatum related to motivation for juice and cocaine rewards. , 1996, Journal of neurophysiology.

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

[39]  Munetaka Shidara,et al.  Differential encoding of information about progress through multi-trial reward schedules by three groups of ventral striatal neurons , 2004, Neuroscience Research.

[40]  Hannah S. Locke,et al.  Prefrontal cortex mediation of cognitive enhancement in rewarding motivational contexts , 2010, Proceedings of the National Academy of Sciences.

[41]  E. Miller,et al.  Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task , 2003, The European journal of neuroscience.