The dual-route hypothesis: evaluating a neurocomputational model of fear conditioning in rats

Research on the neural bases of emotion raises much controversy and few quantitative models exist that can help address the issues raised. Here we replicate and dissect one of those models, Armony and colleagues’ neurocomputational model of fear conditioning, which is based on LeDoux's dual-route hypothesis regarding the rat fear circuitry. The importance of the model's modular abstraction of the neuroanatomy, its use of population coding, and in particular the interplay between thalamo-amygdala and thalamo-cortical pathways are tested. We show that a trivially minimal version of the model can produce conditioning to a reinforced stimulus without recourse to the dual pathway structure, but a modification of the original model, which nevertheless preserves the thalamo-amygdala and (reduced) thalamo-cortical pathways, enables stronger conditioning to a conditioned stimulus. Implications for neurocomputational modelling approaches are discussed.

[1]  B. Balleine,et al.  The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning , 2003, The Journal of Neuroscience.

[2]  Edmund T. Rolls,et al.  What Are Emotions, Why Do We Have Emotions, and What Is Their Computational Basis in the Brain? , 2005, Who Needs Emotions?.

[3]  M. Pringle LEARNING AND EMOTION(1) , 1958 .

[4]  Joseph E LeDoux,et al.  Differential Effects of Amygdala Lesions on Early and Late Plastic Components of Auditory Cortex Spike Trains during Fear Conditioning , 1998, The Journal of Neuroscience.

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

[6]  Joseph E LeDoux Brain mechanisms of emotion and emotional learning , 1992, Current Biology.

[7]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[8]  Christian Balkenius,et al.  EMOTIONAL LEARNING: A COMPUTATIONAL MODEL OF THE AMYGDALA , 2001, Cybern. Syst..

[9]  Stephen Maren,et al.  Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction , 2001, The Journal of Neuroscience.

[10]  Klaus R. Scherer,et al.  Emotion, Development, and Self-Organization: Emotions as Episodes of Subsystem Synchronization Driven by Nonlinear Appraisal Processes , 2000 .

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

[12]  Gianluca Baldassarre,et al.  The Role of Amygdala in Devaluation : A Model Tested with a Simulated Rat , 2007 .

[13]  Jonathan C. Gewirtz,et al.  Is the hippocampus necessary for contextual fear conditioning? , 2000, Behavioural Brain Research.

[14]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Joseph E LeDoux,et al.  Partial disruption of fear conditioning in rats with unilateral amygdala damage: correspondence with unilateral temporal lobectomy in humans. , 1996, Behavioral neuroscience.

[16]  A. Damasio,et al.  Role of the Amygdala in Decision‐Making , 2003, Annals of the New York Academy of Sciences.

[17]  Robert M. Sapolsky,et al.  Stress, Stress-Related Disease, and Emotional Regulation. , 2007 .

[18]  Joseph E LeDoux,et al.  An anatomically constrained neural network model of fear conditioning. , 1995, Behavioral neuroscience.

[19]  J. Edeline,et al.  Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning. , 1992, Behavioral neuroscience.

[20]  Joseph E LeDoux,et al.  Erratum: Organization of intra-amygdaloid circuitries in the rat: An emerging framework for understanding functions of the amygdala (Trends in Neuroscience (Nov. 1997) 20 (517-523)) , 1998 .

[21]  Francesco Mannella,et al.  A Computational Model of the Amygdala Nuclei's Role in Second Order Conditioning , 2008, SAB.

[22]  Timothy J Desmond,et al.  Behavioral / Systems / Cognitive Hippocampal Inactivation Disrupts the Acquisition and Contextual Encoding of Fear Extinction , 2005 .

[23]  James S. Morgan,et al.  A Hierarchical Network of Control Systems that Learn: Modeling Nervous System Function During Classical and Instrumental Conditioning , 1993, Adapt. Behav..

[24]  M. Deschenes,et al.  Anatomical evidence for a mechanism of lateral inhibition in the rat thalamus , 1998, The European journal of neuroscience.

[25]  W. Freeman How Brains Make Up Their Minds , 1999 .

[26]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

[27]  J. Morén,et al.  A computational model of emotional learning in the amygdala. , 2000 .

[28]  Joseph E. LeDoux,et al.  Toward Basic Principles for Emotional Processing , 2005, Who Needs Emotions?.

[29]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[30]  Joseph E. LeDoux,et al.  Emotional Circuits and Computational Neuroscience , 2002 .

[31]  Joseph E LeDoux,et al.  Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala , 1997, Trends in Neurosciences.

[32]  Joseph E LeDoux,et al.  Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats. , 1997, Cerebral cortex.

[33]  Marc D. Lewis Bridging emotion theory and neurobiology through dynamic systems modeling , 2005, Behavioral and Brain Sciences.

[34]  木島 泰三 書評 アントニオ・ダマシオ著『スピノザを探して』(未邦訳)--Antonio Damasio, Looking for Spinoza: Joy, Sorrow, and the Feeling Brain, Harcourt, 2003 , 2005 .

[35]  Joseph E LeDoux,et al.  Response properties of single units in areas of rat auditory thalamus that project to the amygdala , 2004, Experimental Brain Research.

[36]  Anthony F. Morse,et al.  Towards an Enactive Cognitive Architecture , 2008 .

[37]  Jonathan D. Cohen,et al.  Computational modeling of emotion: explorations through the anatomy and physiology of fear conditioning , 1997, Trends in Cognitive Sciences.

[38]  J. H. Curtis,et al.  Learning Theory and Behavior , 1960 .

[39]  D. Lundqvist,et al.  Unconscious emotion : Evolutionary perspectives, psychophysiological data, and neuropsychological mechanisms , 2000 .

[40]  Joseph E. LeDoux,et al.  Toward basic principles for emotional processing: What the fearful brain tells the robot , 2005 .

[41]  Joseph E LeDoux,et al.  Response properties of single units in areas of rat auditory thalamus that project to the amygdala , 1994, Experimental Brain Research.

[42]  P. Petta,et al.  Computational models of emotion , 2010 .

[43]  Joseph E LeDoux Information flow from sensation to emotion: Plasticity in the neural computation of stimulus value. , 1990 .

[44]  P. Young,et al.  Emotion and personality , 1963 .

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

[46]  Tom Ziemke,et al.  On the Role of Emotion in Embodied Cognitive Architectures: From Organisms to Robots , 2009, Cognitive Computation.

[47]  D. Cicchetti Emotion and Adaptation , 1993 .