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The Journal of Neuroscience, July 2, 2008, 28(27):6950-6959; doi:10.1523/JNEUROSCI.1615-08.2008

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Behavioral/Systems/Cognitive
Functional Interaction between the Hippocampus and Nucleus Accumbens Shell Is Necessary for the Acquisition of Appetitive Spatial Context Conditioning

Rutsuko Ito,^1,3 Trevor W. Robbins,¹ Cyriel M. Pennartz,² and Barry J. Everitt¹

¹Department of Experimental Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom, ²Graduate School Neurosciences Amsterdam, University of Amsterdam, Faculty of Science, Swammerdam Institute for Life Sciences, 1098 SM Amsterdam, The Netherlands, and ³Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom

Correspondence should be addressed to Dr. Rutsuko Ito, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, UK. Email: rutsuko.ito{at}psy.ox.ac.uk

The nucleus accumbens (NAc) has been implicated in a variety of associative processes that are dependent on the integrity of the amygdala and hippocampus (HPC). However, the extent to which the two subregions of the NAc, the core and shell, form differentiated circuits within the amygdala- and hippocampal-ventral striatal circuitry remains unclear. The present study investigated the effects of selective excitotoxic lesions of the nucleus accumbens shell or core subregion on appetitive elemental cue and context conditioning, shown previously to be dependent on the basolateral amygdala and hippocampus, respectively. Rats were trained sequentially to acquire discrete conditioned stimulus–sucrose conditioning, followed by spatial context–sucrose conditioning in a place preference apparatus characterized by three topographically identical chambers, the chambers being discriminable only on the basis of path integration. NAc shell lesions selectively impaired the acquisition of conditioned place preference and the use of spatial information to retrieve information about a discrete cue, whereas, as expected, NAc core lesions attenuated the acquisition of cue conditioning compared with sham rats. In a subsequent experiment, disconnection of the HPC from the NAc shell using unilateral asymmetric lesions of each structure resulted in a pattern of impairment in place conditioning and context-dependent cue retrieval similar to that produced by NAc shell lesions. These data not only suggest that the NAc core and shell subregions subserve distinct associative processes but also that the NAc shell and HPC are important functional components of a limbic corticostriatal network involved in spatial context conditioning.

Key words: conditioned place preference; learning and memory systems; hippocampus; amygdala; nucleus accumbens; limbic

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Received Jan. 8, 2008; revised May 27, 2008; accepted May 27, 2008.

Correspondence should be addressed to Dr. Rutsuko Ito, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, UK. Email: rutsuko.ito{at}psy.ox.ac.uk

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