Opposing effects of amygdala and orbital prefrontal cortex lesions on the extinction of instrumental responding in macaque monkeys

Extinction is a well‐known behavioural phenomenon that allows organisms to respond flexibly to a changing environment. Although recent work implicates the amygdala and orbital prefrontal cortex (PFo) in extinction of Pavlovian conditioned fear and aversion, much less is known about the neural bases of instrumental extinction. To explore the contribution of the macaque amygdala to flexible responding in the face of changing reward contingency, we tested the effects of selective, excitotoxic lesions of the amygdala on extinction of an instrumental response. For comparison, we evaluated the effects of ablation of PFo on the same task. Amygdala lesions facilitated the extinction of instrumental responses, whereas lesions of PFo had the opposite effect.

[1]  B. Everitt,et al.  Lesions of the Orbitofrontal but not Medial Prefrontal Cortex Disrupt Conditioned Reinforcement in Primates , 2003, The Journal of Neuroscience.

[2]  D. Gaffan,et al.  Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  E. Murray,et al.  Aspiration lesions of the amygdala disrupt the rhinal corticothalamic projection system in rhesus monkeys , 1998, Experimental Brain Research.

[4]  A. Meyer-Lindenberg,et al.  5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression , 2005, Nature Neuroscience.

[5]  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.

[6]  S. Shelton,et al.  The Primate Amygdala Mediates Acute Fear But Not the Behavioral and Physiological Components of Anxious Temperament , 2001, The Journal of Neuroscience.

[7]  Alicia Izquierdo,et al.  Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys , 2005, The Journal of Neuroscience.

[8]  J. Fuster.  Prefrontal Cortex , 2018 .

[9]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[10]  Bruce Fischl,et al.  Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T. Robbins,et al.  Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala , 1997, Nature.

[12]  K. Pribram,et al.  Learning and limbic lesions , 1966 .

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

[14]  Daniel O'Connor,et al.  Laminar, tangential and regional organization of the noradrenergic innervation of monkey cortex: Dopamine-β-hydroxylase immunohistochemistry , 1982, Brain Research Bulletin.

[15]  Joseph E LeDoux,et al.  Extinction Learning in Humans Role of the Amygdala and vmPFC , 2004, Neuron.

[16]  J. A. McDonald,et al.  Orality, Preference Behavior, and Reinforcement Value of Nonfood Object in Monkeys with Orbital Frontal Lesions , 1969, Science.

[17]  Joseph E LeDoux,et al.  New vistas on amygdala networks in conditioned fear. , 2004, Journal of neurophysiology.

[18]  M. Mishkin,et al.  Conditioning and extinction of a food-rewarded response after selective ablations of frontal cortex in rhesus monkeys. , 1963, Experimental neurology.

[19]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[20]  T. Robbins,et al.  Contrasting Roles of Basolateral Amygdala and Orbitofrontal Cortex in Impulsive Choice , 2004, The Journal of Neuroscience.

[21]  T. Barrett.  Studies of the function of the amygdaloid complex in Macaca Mulatta , 1969 .

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

[23]  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 .

[24]  M. Bouton.  Context, ambiguity, and unlearning: sources of relapse after behavioral extinction , 2002, Biological Psychiatry.

[25]  D. A. Poulos,et al.  Discrimination behavior after amygdalectomy in monkeys: learning set and discrimination reversals. , 1965, Journal of comparative and physiological psychology.

[26]  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.

[27]  E. Murray,et al.  Bilateral Orbital Prefrontal Cortex Lesions in Rhesus Monkeys Disrupt Choices Guided by Both Reward Value and Reward Contingency , 2004, The Journal of Neuroscience.

[28]  P. Holland,et al.  Amygdala–frontal interactions and reward expectancy , 2004, Current Opinion in Neurobiology.

[29]  Alicia Izquierdo,et al.  Combined unilateral lesions of the amygdala and orbital prefrontal cortex impair affective processing in rhesus monkeys. , 2004, Journal of neurophysiology.

[30]  D. Gaffan,et al.  Crossed unilateral lesions of the medial forebrain bundle and either inferior temporal or frontal cortex impair object–reward association learning in Rhesus monkeys , 2001, Neuropsychologia.

[31]  T. Robbins,et al.  Dissociable roles of the central and basolateral amygdala in appetitive emotional learning , 2000, The European journal of neuroscience.

[32]  G. Quirk,et al.  The Role of Ventromedial Prefrontal Cortex in the Recovery of Extinguished Fear , 2000, The Journal of Neuroscience.

[33]  E. Murray,et al.  Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex , 2000, The Journal of Neuroscience.

[34]  J. Nagode,et al.  Double Dissociation of Exteroceptive and Interoceptive Feedback Systems in the Orbital and Ventromedial Prefrontal Cortex of Humans , 2005, The Journal of Neuroscience.

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

[36]  R. Dolan,et al.  Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value , 2004, Nature Neuroscience.

[37]  T. Robbins,et al.  The neuropsychology of ventral prefrontal cortex: Decision-making and reversal learning , 2004, Brain and Cognition.

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

[39]  Charles M. Butter,et al.  Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta , 1969 .

[40]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[41]  D. Paré,et al.  Prefrontal Control of the Amygdala , 2005, The Journal of Neuroscience.

[42]  A C Roberts,et al.  The Role of the Primate Amygdala in Conditioned Reinforcement , 2001, The Journal of Neuroscience.