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

Attentional set-shifting and discrimination reversal are sensitive to prefrontal damage in the marmoset in a manner qualitatively similar to that seen in man and Old World monkeys, respectively (Dias et al., 1996b). Preliminary findings have demonstrated that although lateral but not orbital prefrontal cortex is the critical locus inshifting an attentional set betweenperceptual dimensions, orbital but not lateral prefrontal cortex is the critical locus in reversing a stimulus–reward association within a particular perceptual dimension (Dias et al., 1996a). The present study presents this analysis in full and extends the results in three main ways by demonstrating that (1) mechanisms of inhibitory control and “on-line” processing are independent within the prefrontal cortex, (2) impairments in inhibitory control induced by prefrontal damage are restricted to novel situations, and (3) those prefrontal areas involved in the suppression of previously established response sets are not involved in the acquisition of such response sets. These findings suggest that inhibitory control is a general process that operates across functionally distinct regions within the prefrontal cortex. Although damage to lateral prefrontal cortex causes a loss of inhibitory control in attentional selection, damage to orbitofrontal cortex causes a loss of inhibitory control in affective processing. These findings provide an explanation for the apparent discrepancy between human and nonhuman primate studies in which disinhibition as measured on the Wisconsin Card Sort Test is associated with dorsolateral prefrontal damage, whereas disinhibition as measured on discrimination reversal is associated with orbitofrontal damage.

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

[2]  C. Butter,et al.  Impairments in selective attention to visual stimuli in monkeys with inferotemporal and lateral striate lesions. , 1969, Brain research.

[3]  N. Mackintosh,et al.  Selective attention and response strategies as factors in serial reversal learning. , 1969 .

[4]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[5]  W. Nauta The problem of the frontal lobe: a reinterpretation. , 1971, Journal of psychiatric research.

[6]  N. Mackintosh,et al.  Mechanisms of animal discrimination learning , 1971 .

[7]  C. Gross,et al.  Further analysis of visual discrimination deficits following foveal prestriate and inferotemporal lesions in rhesus monkeys. , 1971, Journal of comparative and physiological psychology.

[8]  J. Fuster Prefrontal Cortex , 2018 .

[9]  R. Lazar,et al.  Effects of frontal lobe lesions on hypothesis sampling during concept formation , 1983, Neuropsychologia.

[10]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[11]  J. Fuster The Prefrontal Cortex and Temporal Integration , 1985 .

[12]  A. Damasio,et al.  Severe disturbance of higher cognition after bilateral frontal lobe ablation , 1985, Neurology.

[13]  A. Damasio,et al.  Severe disturbance of higher cognition after bilateral frontal lobe ablation: Patient EVR , 1986 .

[14]  T. Robbins,et al.  The effects of intradimensional and extradimensional shifts on visual discrimination learning in humans and non-human primates , 1988, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[15]  D. Gaffan,et al.  Amygdalar interaction with the mediodorsal nucleus of the thalamus and the ventromedial prefrontal cortex in stimulus-reward associative learning in the monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  A. Diamond Developmental Time Course in Human Infants and Infant Monkeys, and the Neural Bases of, Inhibitory Control in Reaching a , 1990, Annals of the New York Academy of Sciences.

[17]  T. Shallice,et al.  Deficits in strategy application following frontal lobe damage in man. , 1991, Brain : a journal of neurology.

[18]  T. Robbins,et al.  A specific form of cognitive rigidity following excitotoxic lesions of the basal forebrain in marmosets , 1992, Neuroscience.

[19]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[20]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  T. Robbins,et al.  Contrasting mechanisms of impaired attentional set-shifting in patients with frontal lobe damage or Parkinson's disease. , 1993, Brain : a journal of neurology.

[22]  M. Fabre-Thorpe,et al.  Interaction of the Amygdala with the Frontal Lobe in Reward Memory , 1993, The European journal of neuroscience.

[23]  Tim Shallice,et al.  Supervisory control of action and thought selection. , 1993 .

[24]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[25]  Marcia Grabowecky,et al.  Escape from linear time: Prefrontal cortex and conscious experience , 1995 .

[26]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[27]  A C Roberts,et al.  Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. , 1996, Behavioral neuroscience.

[28]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

[29]  C. Gerfen,et al.  The frontal cortex-basal ganglia system in primates. , 1996, Critical reviews in neurobiology.

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

[31]  M. Petrides,et al.  Specialized systems for the processing of mnemonic information within the primate frontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  R. Passingham,et al.  Ventral Prefrontal Cortex Is Not Essential for Working Memory , 1997, The Journal of Neuroscience.