Neural Correlates of Specific and General Pavlovian-to-Instrumental Transfer within Human Amygdalar Subregions: A High-Resolution fMRI Study

It is widely held that the interaction between instrumental and Pavlovian conditioning induces powerful motivational biases. Pavlovian-Instrumental Transfer (PIT) is one of the key paradigms demonstrating this effect, which can further be decomposed into a general and specific component. Although these two forms of PIT have been studied at the level of amygdalar subregions in rodents, it is still unknown whether they involve different areas of the human amygdala. Using a high-resolution fMRI (hr-fMRI) protocol optimized for the amygdala in combination with a novel free operant task designed to elicit effects of both general and specific PIT, we demonstrate that a region of ventral amygdala within the boundaries of the basolateral complex and the ventrolateral putamen are involved in specific PIT, while a region of dorsal amygdala within the boundaries of the centromedial complex is involved in general PIT. These results add to a burgeoning literature indicating different functional contributions for these different amygdalar subregions in reward-processing and motivation.

[1]  Jean-Philippe Thirion,et al.  Image matching as a diffusion process: an analogy with Maxwell's demons , 1998, Medical Image Anal..

[2]  M. Bradley Natural selective attention: orienting and emotion. , 2009, Psychophysiology.

[3]  Can Ceritoglu,et al.  Increasing the power of functional maps of the medial temporal lobe by using large deformation diffeomorphic metric mapping. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  José M. R. Delgado,et al.  Integrative Activity of the Brain , 1968, The Yale Journal of Biology and Medicine.

[5]  B. Balleine,et al.  The General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer Are Differentially Mediated by the Nucleus Accumbens Core and Shell , 2011, The Journal of Neuroscience.

[6]  B. Balleine,et al.  Double Dissociation of Basolateral and Central Amygdala Lesions on the General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer , 2005, The Journal of Neuroscience.

[7]  B. Balleine,et al.  Parallel incentive processing: an integrated view of amygdala function , 2006, Trends in Neurosciences.

[8]  B. Balleine,et al.  The Neural Mechanisms Underlying the Influence of Pavlovian Cues on Human Decision Making , 2008, The Journal of Neuroscience.

[9]  B. Balleine,et al.  The Role of Learning in the Operation of Motivational Systems , 2002 .

[10]  B. Balleine,et al.  The Role of the Nucleus Accumbens in Instrumental Conditioning: Evidence of a Functional Dissociation between Accumbens Core and Shell , 2001, The Journal of Neuroscience.

[11]  Denis Dooley,et al.  Atlas of the Human Brain. , 1971 .

[12]  D. Garner,et al.  The Eating Attitudes Test: psychometric features and clinical correlates , 1982, Psychological Medicine.

[13]  Nicholas Ayache,et al.  Non-parametric Diffeomorphic Image Registration with the Demons Algorithm , 2007, MICCAI.

[14]  P. Dayan,et al.  Human Pavlovian–Instrumental Transfer , 2008, The Journal of Neuroscience.

[15]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[16]  Michael A Yassa,et al.  A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe , 2009, NeuroImage.

[17]  B. C. Lacey,et al.  Pupillary and cardiac activity during visual attention. , 1973, Psychophysiology.

[18]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[19]  G. Hall,et al.  Lesions of the Basolateral Amygdala Disrupt Selective Aspects of Reinforcer Representation in Rats , 2001, The Journal of Neuroscience.

[20]  Ryan K. Jessup,et al.  Differentiable contributions of human amygdalar subregions in the computations underlying reward and avoidance learning , 2011, The European journal of neuroscience.

[21]  A. Dickinson,et al.  Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour , 2001, The European journal of neuroscience.

[22]  P. Holland,et al.  Double dissociation of the effects of lesions of basolateral and central amygdala on conditioned stimulus‐potentiated feeding and Pavlovian‐instrumental transfer , 2003, The European journal of neuroscience.

[23]  C. Mathias,et al.  Skin vasomotor reflex responses in two contrasting groups of autonomic failure , 2006, Journal of Neurology.

[24]  P. Holland Relations between Pavlovian-instrumental transfer and reinforcer devaluation. , 2004, Journal of experimental psychology. Animal behavior processes.

[25]  D. Barnes-Holmes,et al.  Children's emergent preferences for soft drinks: Stimulus-equivalence and transfer , 2003 .

[26]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[27]  Anna Rose Childress,et al.  Conditioning factors in drug abuse: can they explain compulsion? , 1998, Journal of psychopharmacology.