Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex

Goal-directed actions are guided by expected outcomes of those actions. Humans with bilateral damage to ventromedial prefrontal cortex, or the amygdala, are deficient in their ability to use information about positive and negative outcomes to guide their choice behavior. Similarly, rats and monkeys with orbital prefrontal or amygdala damage have been found to be impaired in their responses to changing values of outcomes. In the present study, we tested whether direct, functional interaction between the amygdala and the orbital prefrontal cortex is necessary for guiding behavior based on expected outcomes. Unlike control monkeys, rhesus monkeys with surgical disconnection of these two structures, achieved by crossed unilateral lesions of the amygdala in one hemisphere and orbital prefrontal cortex in the other, combined with forebrain commissurotomy, were unable to adjust their choice behavior after a change in the outcome (here, a reduction in the value of a particular reinforcer). The lesions did not affect motivation to work for a food reinforcer, or food preferences, per se. Hence, the amygdala and orbital prefrontal cortex act as part of an integrated neural system guiding decision-making and adaptive response selection.

[1]  L. Weiskrantz,et al.  Behavioral changes associated with ablation of the amygdaloid complex in monkeys. , 1956, Journal of comparative and physiological psychology.

[2]  G. Ettlinger.  Visual discrimination following successive temporal ablations in monkeys. , 1959, Brain : a journal of neurology.

[3]  H. Teuber,et al.  Unity and diversity of frontal lobe functions. , 1972, Acta neurobiologiae experimentalis.

[4]  R. Passingham,et al.  Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). , 1981, Journal of comparative and physiological psychology.

[5]  P. Goldman-Rakic,et al.  Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys , 1981, The Journal of comparative neurology.

[6]  R. Passingham,et al.  An assessment of the reinforcing properties of foods after amygdaloid lesions in rhesus monkeys. , 1982, Journal of comparative and physiological psychology.

[7]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[8]  N. Hiroi,et al.  The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  T. Robbins,et al.  Amygdala-ventral striatal interactions and reward-related processes. , 1992 .

[10]  Michael Davis,et al.  The role of the amygdala in conditioned fear. , 1992 .

[11]  E. Lauterbach.  The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1993 .

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

[13]  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.

[14]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[15]  Joseph E LeDoux.  Emotion: clues from the brain. , 1995, Annual review of psychology.

[16]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

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

[18]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.

[19]  R. W. Flint,et al.  Anterior rhinal cortex and amygdala: dissociation of their contributions to memory and food preference in rhesus monkeys. , 1996, Behavioral neuroscience.

[20]  E. Murray,et al.  Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys , 1997, The Journal of Neuroscience.

[21]  R. Adolphs,et al.  The human amygdala in social judgment , 1998, Nature.

[22]  H. Damasio,et al.  Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex , 1998, The Journal of Neuroscience.

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

[24]  E. Murray,et al.  Rhinal cortex ablations fail to disrupt reinforcer devaluation effects in rhesus monkeys (Macaca mulatta). , 1998, Behavioral neuroscience.

[25]  M Meunier,et al.  Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys , 1999, The European journal of neuroscience.

[26]  Hanna Damasio,et al.  Impairment of social and moral behavior related to early damage in human prefrontal cortex , 1999, Nature Neuroscience.

[27]  G. Schoenbaum,et al.  Orbitofrontal Cortex and Representation of Incentive Value in Associative Learning , 1999, The Journal of Neuroscience.

[28]  A C Roberts,et al.  Performance norms for a rhesus monkey neuropsychological testing battery: acquisition and long-term performance. , 1999, Brain research. Cognitive brain research.

[29]  P. Holland,et al.  Amygdala circuitry in attentional and representational processes , 1999, Trends in Cognitive Sciences.

[30]  T. Robbins,et al.  Choosing between Small, Likely Rewards and Large, Unlikely Rewards Activates Inferior and Orbital Prefrontal Cortex , 1999, The Journal of Neuroscience.

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

[32]  T. Robbins,et al.  Dissociable Deficits in the Decision-Making Cognition of Chronic Amphetamine Abusers, Opiate Abusers, Patients with Focal Damage to Prefrontal Cortex, and Tryptophan-Depleted Normal Volunteers: Evidence for Monoaminergic Mechanisms , 1999, Neuropsychopharmacology.

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

[34]  Gregory P. Lee,et al.  Different Contributions of the Human Amygdala and Ventromedial Prefrontal Cortex to Decision-Making , 1999, The Journal of Neuroscience.

[35]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

[36]  R. Passingham,et al.  Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning , 2000, Experimental Brain Research.