Interaction of Insular Cortex and Ventral Striatum Mediates the Effect of Incentive Memory on Choice Between Goal-Directed Actions

The anterior insular cortex (IC) and the nucleus accumbens (NAc) core have been separately implicated in the selection and performance of actions based on the incentive value of the instrumental outcome. Here, we examined the role of connections between the IC and the NAc core in the performance of goal-directed actions. Rats were trained on two actions for distinct outcomes, after which one of the two outcomes was devalued by specific satiety immediately before a choice extinction test. We first confirmed the projection from the IC to the NAc core and then disconnected these structures via asymmetrical excitotoxic lesions before training. Contralateral, but not ipsilateral, disconnection of the IC and NAc core disrupted outcome devaluation. We hypothesized that communication between the IC and NAc core is necessary for the retrieval of incentive value at test. To test this, we infused the GABAA agonist muscimol into the IC and the μ-opioid receptor antagonist CTAP into the contralateral NAc before the choice extinction test. As expected, inactivation of the IC in one hemisphere and blocking μ-opioid receptors in the contralateral NAc core abolished outcome-selective devaluation. These results suggest that the IC and NAc core form part of a circuit mediating the retrieval of outcome values and the subsequent choice between goal-directed actions based on those values.

[1]  M. Roesch,et al.  From ventral-medial to dorsal-lateral striatum: Neural correlates of reward-guided decision-making , 2015, Neurobiology of Learning and Memory.

[2]  Bernard W Balleine,et al.  The Role of the Amygdala-Striatal Pathway in the Acquisition and Performance of Goal-Directed Instrumental Actions , 2013, The Journal of Neuroscience.

[3]  E. Levin,et al.  Role of insular cortex D1 and D2 dopamine receptors in nicotine self-administration in rats , 2013, Behavioural Brain Research.

[4]  Shauna L. Parkes,et al.  Incentive Memory: Evidence the Basolateral Amygdala Encodes and the Insular Cortex Retrieves Outcome Values to Guide Choice between Goal-Directed Actions , 2013, The Journal of Neuroscience.

[5]  B. Balleine,et al.  μ- and δ-Opioid-Related Processes in the Accumbens Core and Shell Differentially Mediate the Influence of Reward-Guided and Stimulus-Guided Decisions on Choice , 2012, The Journal of Neuroscience.

[6]  Viviana Trezza,et al.  Nucleus Accumbens μ-Opioid Receptors Mediate Social Reward , 2011, The Journal of Neuroscience.

[7]  JaneR . Taylor,et al.  Dissociable regulation of instrumental action within mouse prefrontal cortex , 2010, The European journal of neuroscience.

[8]  B. Balleine,et al.  At the limbic–motor interface: disconnection of basolateral amygdala from nucleus accumbens core and shell reveals dissociable components of incentive motivation , 2010, The European journal of neuroscience.

[9]  A. Bechara,et al.  The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making , 2010, Brain Structure and Function.

[10]  B. Balleine,et al.  Acquisition and Performance of Goal-Directed Instrumental Actions Depends on ERK Signaling in Distinct Regions of Dorsal Striatum in Rats , 2010, The Journal of Neuroscience.

[11]  E. Coutureau,et al.  Transient role of the rat prelimbic cortex in goal‐directed behaviour , 2009, The European journal of neuroscience.

[12]  Antoine Bechara,et al.  The hidden island of addiction: the insula , 2009, Trends in Neurosciences.

[13]  E. Unterwald,et al.  Cocaine reward and hyperactivity in the rat: Sites of mu opioid receptor modulation , 2008, Neuroscience.

[14]  P. Fuchs,et al.  GABAA but not GABAB receptors in the rostral anterior cingulate cortex selectively modulate pain-induced escape/avoidance behavior , 2007, Experimental Neurology.

[15]  D. S. Zahm,et al.  Specificity in the Projections of Prefrontal and Insular Cortex to Ventral Striatopallidum and the Extended Amygdala , 2005, The Journal of Neuroscience.

[16]  B. Balleine,et al.  Lesions of Medial Prefrontal Cortex Disrupt the Acquisition But Not the Expression of Goal-Directed Learning , 2005, The Journal of Neuroscience.

[17]  B. Balleine,et al.  The role of the dorsomedial striatum in instrumental conditioning , 2005, The European journal of neuroscience.

[18]  Paul Leonard Gabbott,et al.  Areal and synaptic interconnectivity of prelimbic (area 32), infralimbic (area 25) and insular cortices in the rat , 2003, Brain Research.

[19]  B. Balleine,et al.  The role of prelimbic cortex in instrumental conditioning , 2003, Behavioural Brain Research.

[20]  S. Killcross,et al.  Coordination of actions and habits in the medial prefrontal cortex of rats. , 2003, Cerebral cortex.

[21]  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.

[22]  B. Balleine,et al.  The Effect of Lesions of the Insular Cortex on Instrumental Conditioning: Evidence for a Role in Incentive Memory , 2000, The Journal of Neuroscience.

[23]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[24]  B. Balleine,et al.  The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety , 1998 .

[25]  Suzanne N. Haber,et al.  Insular Cortical Projections to Functional Regions of the Striatum Correlate with Cortical Cytoarchitectonic Organization in the Primate , 1997, The Journal of Neuroscience.

[26]  H. Groenewegen,et al.  Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat , 1996, Neuroscience.

[27]  B. Balleine,et al.  Motivational control of goal-directed action , 1994 .

[28]  A. McDonald,et al.  Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain , 1991, Neuroscience.

[29]  C. Saper,et al.  Organization of visceral and limbic connections in the insular cortex of the rat , 1991, The Journal of comparative neurology.

[30]  W. Nauta,et al.  The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods , 1982, Neuroscience.