The role of the amygdala and rostral anterior cingulate in encoding expected outcomes during learning

Successful passive avoidance learning is thought to require the use of learned stimulus-reinforcement associations to guide decision making [Baxter, M.G., Murray, E.A., 2002. The amygdala and reward. Nature Reviews. Neuroscience 3, 563-573]. The current experiment investigated the neural correlates of successful passive avoidance learning in 19 healthy adults. Behaviorally, subjects showed a distinct pattern of performance: early indiscriminate responding to stimuli (pre-criterion performance), followed by relatively rapid learning before a plateau of successful performance (post-criterion performance). Neural responses to post-criterion correct responses were compared with neural responses to both incorrect responses and pre-criterion correct responses. Post-criterion correct responding was associated with increased activation in regions including rostral anterior cingulate, insula, caudate, hippocampal regions, and the amygdala.

[1]  Derek G. V. Mitchell,et al.  Passive avoidance learning in individuals with psychopathy: modulation by reward but not by punishment , 2004 .

[2]  R. Blair,et al.  Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy , 2001, Journal of neurology, neurosurgery, and psychiatry.

[3]  D. Lykken,et al.  A study of anxiety in the sociopathic personality. , 1957, Journal of abnormal psychology.

[4]  Lisa M Shin,et al.  Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study , 2000, Biological Psychiatry.

[5]  G. Schoenbaum,et al.  Neural Encoding in Ventral Striatum during Olfactory Discrimination Learning , 2003, Neuron.

[6]  Karl J. Friston,et al.  Temporal Difference Models and Reward-Related Learning in the Human Brain , 2003, Neuron.

[7]  P. Montague,et al.  Activity in human ventral striatum locked to errors of reward prediction , 2002, Nature Neuroscience.

[8]  K. Kiehl,et al.  Event‐related fMRI study of response inhibition , 2001, Human brain mapping.

[9]  P R Sanberg,et al.  Cholinergic lesion of the striatum impairs acquisition and retention of a passive avoidance response. , 1984, Behavioral neuroscience.

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

[11]  David M. Bannerman,et al.  Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery , 2002, Behavioural Brain Research.

[12]  Morten L Kringelbach,et al.  Methamphetamine Activates Reward Circuitry in Drug Naïve Human Subjects , 2004, Neuropsychopharmacology.

[13]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[14]  G. Tassoni,et al.  Neural Topography and Chronology of Memory Consolidation: A Review of Functional Inactivation Findings , 1999, Neurobiology of Learning and Memory.

[15]  Lisa M Shin,et al.  Neuroimaging Studies of Amygdala Function in Anxiety Disorders , 2003, Annals of the New York Academy of Sciences.

[16]  James L. McGaugh,et al.  Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion , 1991, Brain Research.

[17]  M. Raichle,et al.  Subgenual prefrontal cortex abnormalities in mood disorders , 1997, Nature.

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

[19]  S. Rauch,et al.  Functional Neuroimaging Studies in Posttraumatic Stress Disorder , 1997, Annals of the New York Academy of Sciences.

[20]  Peter Dayan,et al.  Temporal difference models describe higher-order learning in humans , 2004, Nature.

[21]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[22]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[23]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[24]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[25]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[26]  D. Treit,et al.  Dissociations among the anxiolytic effects of septal, hippocampal, and amygdaloid lesions , 1997 .

[27]  T. Robbins,et al.  Contrasting Cortical and Subcortical Activations Produced by Attentional-Set Shifting and Reversal Learning in Humans , 2000, Journal of Cognitive Neuroscience.

[28]  Geoffrey Schoenbaum,et al.  A systems approach to orbitofrontal cortex function: recordings in rat orbitofrontal cortex reveal interactions with different learning systems , 2003, Behavioural Brain Research.

[29]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[30]  D S Kosson,et al.  Passive avoidance learning in psychopathic and nonpsychopathic offenders. , 1986, Journal of abnormal psychology.

[31]  E. Rolls.  The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[32]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[33]  J. D. McGaugh.  Memory consolidation and the amygdala: a systems perspective , 2002, Trends in Neurosciences.

[34]  Hiroshi Fukuda,et al.  The human prefrontal and parietal association cortices are involved in NO-GO performances—an event-related fMRI study , 2000, NeuroImage.

[35]  Trevor W Robbins,et al.  Appetitive Behavior , 2003, Annals of the New York Academy of Sciences.

[36]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[37]  R. Blair,et al.  The roles of orbital frontal cortex in the modulation of antisocial behavior , 2004, Brain and Cognition.

[38]  N. Ramnani,et al.  Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition , 2004, Biological Psychiatry.

[39]  Adrianna Mendrek,et al.  Limbic abnormalities in affective processing by criminal psychopaths as revealed by functional magnetic resonance imaging , 2001, Biological Psychiatry.

[40]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[41]  M. Delgado,et al.  Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations , 2003, Cognitive, affective & behavioral neuroscience.

[42]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[43]  Benedetto Sacchetti,et al.  Role of ventral hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response memory trace , 1997, Brain Research.

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

[45]  D. Treit,et al.  Effects of centrally administered anxiolytic compounds in animal models of anxiety , 1999, Neuroscience & Biobehavioral Reviews.

[46]  R. Blair,et al.  Neurobiological basis of psychopathy. , 2003, The British journal of psychiatry : the journal of mental science.

[47]  Sylvia M. L. Cox,et al.  Learning to Like: A Role for Human Orbitofrontal Cortex in Conditioned Reward , 2005, The Journal of Neuroscience.

[48]  Y. Miyashita,et al.  No‐go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging , 1998, The European journal of neuroscience.

[49]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[50]  Scott L Rauch,et al.  Functional magnetic resonance imaging: application to posttraumatic stress disorder. , 2003, The Journal of neuropsychiatry and clinical neurosciences.

[51]  T. Braver,et al.  Sensitivity of prefrontal cortex to changes in target probability: A functional MRI study , 2001, Human brain mapping.

[52]  W. Schultz,et al.  Modifications of reward expectation-related neuronal activity during learning in primate orbitofrontal cortex. , 2000, Journal of neurophysiology.

[53]  J. Gray,et al.  The psychology of fear and stress , 1971 .

[54]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[55]  Time-Dependent Deficits of Rat′s Memory Consolidation Induced by Tetrodotoxin Injections into the Caudate-Putamen, Nucleus Accumbens, and Globus Pallidus , 1995, Neurobiology of Learning and Memory.

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

[57]  J. Rawlins,et al.  Effects of medial prefrontal cortex cytotoxic lesions in mice , 2003, Behavioural Brain Research.

[58]  Rebecca Elliott,et al.  Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems , 2004, NeuroImage.