A Comparison of Abstract Rules in the Prefrontal Cortex, Premotor Cortex, Inferior Temporal Cortex, and Striatum

The ability to use abstract rules or principles allows behavior to generalize from specific circumstances. We have previously shown that such rules are encoded in the lateral prefrontal cortex (PFC) and premotor cortex (PMC). Here, we extend these investigations to two other areas directly connected with the PFC and the PMC, the inferior temporal cortex (ITC) and the dorsal striatum (STR). Monkeys were trained to use two abstract rules: same or different. They had to either hold or release a lever, depending on whether two successively presented pictures were the same or different, and depending on which rule was in effect. The rules and the behavioral responses were reflected most strongly and, on average, tended to be earlier in the PMC followed by the PFC and then the STR; few neurons in the ITC reflected the rules or the actions. By contrast, perceptual information (the identity of the pictures used as sample and test stimuli) was encoded more strongly and earlier in the ITC, followed by the PFC; they had weak, if any, effects on neural activity in the PMC and STR. These findings are discussed in the context of the anatomy and posited functions of these areas.

[1]  Y. Cohen,et al.  Neural and behavioral correlates of auditory categorization , 2007, Hearing Research.

[2]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[3]  Narender Ramnani,et al.  Cerebellar contributions to working memory , 2007, NeuroImage.

[4]  E. Miller,et al.  From rule to response: neuronal processes in the premotor and prefrontal cortex. , 2003, Journal of neurophysiology.

[5]  R. Knight Decreased response to novel stimuli after prefrontal lesions in man. , 1984, Electroencephalography and clinical neurophysiology.

[6]  H. Nelson A Modified Card Sorting Test Sensitive to Frontal Lobe Defects , 1976, Cortex.

[7]  David J. Freedman,et al.  Representation of the Quantity of Visual Items in the Primate Prefrontal Cortex , 2002, Science.

[8]  T. Shallice Specific impairments of planning. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[10]  Andrew R. Mitz,et al.  Prefrontal Cortex Activity Related to Abstract Response Strategies , 2005, Neuron.

[11]  D. Pandya,et al.  Frontal lobe connections of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[12]  Bernd Weber,et al.  Amygdala tractography predicts functional connectivity and learning during feedback-guided decision-making , 2008, NeuroImage.

[13]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[14]  M. D’Esposito,et al.  Frontal Networks for Learning and Executing Arbitrary Stimulus-Response Associations , 2005, The Journal of Neuroscience.

[15]  D. Stuss,et al.  Wisconsin Card Sorting Test performance in patients with focal frontal and posterior brain damage: effects of lesion location and test structure on separable cognitive processes , 2000, Neuropsychologia.

[16]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[17]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[18]  A. McIntosh,et al.  Time course of changes in brain activity and functional connectivity associated with long-term adaptation to a rotational transformation. , 2005, Journal of neurophysiology.

[19]  G Winocur,et al.  Prefrontal cortex and caudate nucleus in conditional associative learning: dissociated effects of selective brain lesions in rats. , 1998, Behavioral neuroscience.

[20]  T. Bussey,et al.  Role of prefrontal cortex in a network for arbitrary visuomotor mapping , 2000, Experimental Brain Research.

[21]  David J. Freedman,et al.  The prefrontal cortex: categories, concepts and cognition. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  B. Milner Effects of Different Brain Lesions on Card Sorting: The Role of the Frontal Lobes , 1963 .

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

[24]  S. Wise,et al.  Comparison of learning‐related neuronal activity in the dorsal premotor cortex and striatum , 2004, The European journal of neuroscience.

[25]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Hollerman,et al.  Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior. , 2000, Progress in brain research.

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

[28]  Verónica Nácher,et al.  Neural correlates of a postponed decision report , 2007, Proceedings of the National Academy of Sciences.

[29]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[30]  H. Barbas Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.

[31]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[32]  R. Passingham,et al.  Neural correlates of visuomotor associations. Spatial rules compared with arbitrary rules. , 2001, Experimental brain research.

[33]  R. Passingham,et al.  Cortico‐basal ganglia pathways are essential for the recall of well–established visuomotor associations , 2004, The European journal of neuroscience.

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

[35]  T. Bussey,et al.  Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. , 2002, Behavioral neuroscience.

[36]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

[37]  T. Robbins,et al.  Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man , 1991, Neuropsychologia.

[38]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[39]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[40]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[41]  Tim Shallice,et al.  The Involvement of the Frontal Lobes in Cognitive Estimation , 1978, Cortex.

[42]  L. Goldstein The frontal lobes and voluntary action , 1996 .

[43]  S. Wise,et al.  Rule-dependent neuronal activity in the prefrontal cortex , 1999, Experimental Brain Research.