Integration of Cognitive and Motivational Information in the Primate Lateral Prefrontal Cortex

Abstract:  The prefrontal cortex (PFC), particularly the lateral prefrontal cortex (LPFC), has an important role in cognitive information processing. The area receives projections from sensory association cortices and sends outputs to motor‐related areas. Neurons in LPFC code the behavioral significance of stimuli, which can be abstract precursors for complex motor commands and are structured hierarchically. Loss of these neurons leads to a lack of flexibility in decision making, such as seen in stereotyped behaviors. However, to make more appropriate decisions the code for behavioral significance has to reflect the subject's own desires and demands. Indeed, LPFC has connections with reward‐related areas, such as the orbitofrontal cortex (OFC), basal ganglia, and medial prefrontal cortex. Recently, many studies have reported reward modulation of neural codes of behavioral significance. Using an asymmetric reward paradigm, we can investigate the functional specificity of LPFC neurons that code both cognitive information and motivational information. In this review, we will discuss details of neuronal properties of LPFC neurons from the viewpoints of cognitive information processing and motivational information processing, and the question of how these two pieces of information are integrated. Abstract coding and contextual representations in the cognitive information processing are functional characteristics of LPFC. Such functional specificity in LPFC cognitive processes is supported by a long‐term scale of reward history in the motivational information processing. The integration enables us to make an elaborate decision with respect to goal‐directed behavior in complex circumstances.

[1]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[2]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[3]  T. Ono,et al.  Activity and distribution of learning-related neurons in monkey (Macaca fuscata) prefrontal cortex. , 1990, Behavioral neuroscience.

[4]  N Butters,et al.  Retention of Delayed-Alternation: Effect of Selective Lesions of Sulcus Principalis , 1969, Science.

[5]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[6]  H. Komatsu,et al.  Prefrontal unit activity during a color discrimination task with GO and NO-GO responses in the monkey , 1982, Brain Research.

[7]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[8]  Xiaofeng Lu,et al.  Organization of Multisynaptic Inputs from Prefrontal Cortex to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Rabies Virus , 2005, The Journal of Neuroscience.

[9]  D. Barraclough,et al.  Prefrontal cortex and decision making in a mixed-strategy game , 2004, Nature Neuroscience.

[10]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[11]  E. Perret.  The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. , 1974, Neuropsychologia.

[12]  Functional significance of delay-period activity of primate prefrontal neurons in relation to spatial working memory and reward/omission-of-reward expectancy , 2005, Experimental Brain Research.

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

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

[15]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

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

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

[18]  H. Spinnler.  The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

[19]  M. Mishkin,et al.  Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity , 1970, Experimental Brain Research.

[20]  Okihide Hikosaka,et al.  Functional differences between macaque prefrontal cortex and caudate nucleus during eye movements with and without reward , 2006, Experimental Brain Research.

[21]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[22]  R. Douglas,et al.  Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades , 2004, Experimental Brain Research.

[23]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[24]  K Tsutsui,et al.  Interference from irrelevant features on visual discrimination by macaques (Macaca fuscata): a behavioral analogue of the human Stroop effect. , 2000, Journal of experimental psychology. Animal behavior processes.

[25]  Richard Passingham,et al.  Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta) , 1975, Brain Research.

[26]  H Niki,et al.  Prefrontal unit activity during delayed alternation in the monkey. II. Relation to absolute versus relative direction of response. , 1974, Brain research.

[27]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[28]  N. P. Bichot,et al.  Visual feature selectivity in frontal eye fields induced by experience in mature macaques , 1996, Nature.

[29]  W. Schultz,et al.  Influences of Rewarding and Aversive Outcomes on Activity in Macaque Lateral Prefrontal Cortex , 2006, Neuron.

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

[31]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[32]  D. Pandya,et al.  Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey , 1982, The Journal of comparative neurology.

[33]  Masataka Watanabe,et al.  Prefrontal unit activity during delayed conditional Go/No-go discrimination in the monkey. I. Relation to the stimulus , 1986, Brain Research.

[34]  H. Niki,et al.  Encoding of behavioral significance of visual stimuli by primate prefrontal neurons: relation to relevant task conditions , 2004, Experimental Brain Research.

[35]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[36]  T. Robbins,et al.  Decision-making processes following damage to the prefrontal cortex. , 2002, Brain : a journal of neurology.

[37]  O. Hikosaka,et al.  Comparison of Reward Modulation in the Frontal Eye Field and Caudate of the Macaque , 2006, The Journal of Neuroscience.

[38]  M. Cole.  The Frontal Granular Cortex and Behavior. , 1964 .

[39]  R. Beauchamp.  VISION, MEMORY, AND THE TEMPORAL LOBE , 1991 .

[40]  Samuel M. McClure,et al.  Separate Neural Systems Value Immediate and Delayed Monetary Rewards , 2004, Science.

[41]  Saori C. Tanaka,et al.  Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops , 2004, Nature Neuroscience.

[42]  B. Pillon,et al.  Human autonomy and the frontal lobes. Part I: Imitation and utilization behavior: A neuropsychological study of 75 patients , 1986, Annals of neurology.

[43]  Leslie G. Ungerleider,et al.  Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys , 2004, Experimental Brain Research.

[44]  J. Fuster,et al.  Prefrontal representation of stimulus attributes during delay tasks. II. The role of behavioral significance , 1988, Brain Research.

[45]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[46]  Walle J. H. Nauta,et al.  Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey , 1976, Brain Research.

[47]  D. Pandya,et al.  Anatomic Organization of the Basilar Pontine Projections from Prefrontal Cortices in Rhesus Monkey , 1997, The Journal of Neuroscience.

[48]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

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

[50]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[51]  D. Pandya,et al.  Fiber system linking the mid‐dorsolateral frontal cortex with the retrosplenial/presubicular region in the rhesus monkey , 1999, The Journal of comparative neurology.

[52]  Masamichi Sakagami,et al.  The hierarchical organization of decision making in the primate prefrontal cortex , 1999, Neuroscience Research.

[53]  M. Sakagami,et al.  Spatial selectivity of go/no-go neurons in monkey prefrontal cortex , 2004, Experimental Brain Research.

[54]  E. Drewe.  Go - No Go Learning After Frontal Lobe Lesions in Humans , 1975, Cortex.

[55]  O. Hikosaka,et al.  Responses to task-irrelevant visual features by primate prefrontal neurons. , 2001, Journal of neurophysiology.

[56]  Masataka Watanabe,et al.  Prefrontal unit activity during delayed conditional Go/No-go discrimination in the monkey. II. Relation to Go and No-go responses , 1986, Brain Research.

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

[58]  Okihide Hikosaka,et al.  A Code for Behavioral Inhibition on the Basis of Color, But Not Motion, in Ventrolateral Prefrontal Cortex of Macaque Monkey , 2001, The Journal of Neuroscience.

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

[60]  H. Niki.  Differential activity of prefrontal units during right and left delayed response trials. , 1974, Brain research.

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

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

[63]  N. Butters,et al.  Behavioral effects of sequential and one-stage ablations of orbital prefrontal cortex in the monkey. , 1973, Experimental neurology.

[64]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[65]  J. Kaas,et al.  Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys , 1992, The Journal of comparative neurology.