The Effect of Lesions of the Insular Cortex on Instrumental Conditioning: Evidence for a Role in Incentive Memory

In three experiments, we assessed the effect of lesions aimed at the gustatory region of the insular cortex on instrumental conditioning in rats. In experiment 1, the lesion had no effect on the acquisition of either lever pressing or chain pulling in food-deprived rats whether these actions earned food pellets or a maltodextrin solution. The lesion did, however, attenuate the impact of outcome devaluation, induced by sensory-specific satiety, on instrumental performance but only when assessed in an extinction test. This effect was not secondary to an impairment in instrumental learning; in experiment 2, no evidence was found to suggest that the lesioned rats differed from shams in their ability to encode the specific action-outcome contingencies to which they were exposed during training. In experiment 3, however, lesioned rats were found to be insensitive to the impact of an incentive learning treatment conducted when they were undeprived; although, again, this deficit was confined to a test conducted in extinction. These results are consistent with the view that, in instrumental conditioning, the gustatory region of the insular cortex is involved in encoding the taste of food outcomes in memory and, hence, in encoding the incentive value assigned to these outcomes on the basis of prevailing motivational conditions.

[1]  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.

[2]  S. Kiefer,et al.  The gustatory neocortex of the rat , 1982 .

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

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

[5]  W. Brown Animal Intelligence: Experimental Studies , 1912, Nature.

[6]  Taste agnosia following gustatory neocortex ablation: dissociation from odor and generality across taste qualities. , 1984, Behavioral neuroscience.

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

[8]  D. Meyer The cerebral cortex: Its roles in memory storage and remembering , 1984 .

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

[10]  B. Balleine,et al.  Role of cholecystokinin in the motivational control of instrumental action in rats. , 1994, Behavioral neuroscience.

[11]  Edmund Rolls,et al.  Neural processing related to feeding in primates. , 1994 .

[12]  A. Dickinson,et al.  Reinforcer specificity of the suppression of instrumental performance on a non-contingent schedule , 1989, Behavioural Processes.

[13]  B. Balleine,et al.  The Role of the Hippocampus in Instrumental Conditioning , 2000, The Journal of Neuroscience.

[14]  L. J. Hammond The effect of contingency upon the appetitive conditioning of free-operant behavior. , 1980, Journal of the experimental analysis of behavior.

[15]  R. Rescorla,et al.  Postconditioning devaluation of a reinforcer affects instrumental responding. , 1985 .

[16]  K. Sripanidkulchai,et al.  The cortical projection of the basolateral amygdaloid nucleus in the rat: A retrograde fluorescent dye study , 1984, The Journal of comparative neurology.

[17]  H. Grill,et al.  Gustatory cortex in the rat. I. Physiological properties and cytoarchitecture , 1986, Brain Research.

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

[19]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[20]  R. Rescorla,et al.  Associative Structures In Instrumental Learning , 1986 .

[21]  B. Balleine Instrumental performance following a shift in primary motivation depends on incentive learning. , 1992, Journal of experimental psychology. Animal behavior processes.

[22]  J W Donahoe,et al.  A selectionist approach to reinforcement. , 1993, Journal of the experimental analysis of behavior.

[23]  H. Grill,et al.  Gustatory cortex in the rat. II. Thalamocortical projections , 1986, Brain Research.

[24]  T. Robbins,et al.  Neurobehavioural mechanisms of reward and motivation , 1996, Current Opinion in Neurobiology.