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. 2008 Jul 2;28(27):6950-9.
doi: 10.1523/JNEUROSCI.1615-08.2008.

Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning

Rutsuko Ito  1 , Trevor W Robbins, Cyriel M Pennartz, Barry J Everitt
Affiliations

Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning

Rutsuko Ito et al. J Neurosci. .

Abstract

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.

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Figures

Figure 1.
Figure 1.
Cue and spatial context conditioning task. Cue conditioning: rats were presented with 30 CS–US pairings/session on a variable interval 20–60 s schedule. For the first three sessions, the CS–US presentations were confined to the three wells in one chamber each day, with the starting chamber counterbalanced across rats (e.g., day 1, chamber 1; day 2, chamber 2; day 3, chamber 3). In the second phase (sessions 4–6), the 30 CS–US presentations could be located in any one of nine possible well locations within the place preference apparatus in each trial. Spatial context conditioning: rats were trained to learn that CSs presented in one of three places (chambers) were associated with the sucrose reward, but that CSs presented in the other two places were not. As before, each daily session involved the presentation of 30 CSs presented in random order between the nine possible locations on a VI 20–60 s schedule. This time, however, only the CSs presented in a preassigned positive chamber (n = 10) were rewarded. The other 20 CS presentations were no longer associated with reward. A schematic diagram of one chamber of the apparatus is shown in the bottom right, depicting the locations of the reference light, chamber light, and CS light. Note that only one of the three trays plus CS lights, present in the chamber, has been represented.
Figure 2.
Figure 2.
Schematic representation of quinolinic lesions of the NAc core, NMDA lesions of the NAc shell (left), and disconnection lesions of the NAc shell and HPC (right). Areas shaded in gray and black represent the largest and smallest extent of neuronal damage in a single animal, respectively.
Figure 3.
Figure 3.
Representative photomicrographs of NeuN-stained and cresyl violet-stained coronal sections of rats with NAc shell, core lesions, or sham-operated controls. A, NeuN-stained section through the NAc region of a sham control rat, showing the region of the NAc shell, core, and anterior commissure (ac). B, NeuN-stained section of a NAc shell lesion, showing the complete loss of cell body NeuN immunoreactivity in the shell region and preservation of neurons in the core region. C, Nissl-stained section of a NAc core sham rat showing the tract of the injector (a), as well as boundary of the NAc core. D, Nissl-stained section of a NAc core lesion; marked gliosis can be seen in the areas surrounding the anterior commissure. Marked shrinkage in area (b) dorsolateral to the commissure and the apparent medial shift of the anterior commissure are the result of the loss of neurons in the core region.
Figure 4.
Figure 4.
Mean ± SEM performance of sham-operated controls and NAc core or shell lesion groups in discrete cue conditioning: A, acquisition expressed as number of approaches to the CS within 15 s (correct trial); B, latency to approach CS–US in correct trials; C, locomotor activity; D, general nose-poke activity. NAcC, NAc core; NAcSh, NAc shell.
Figure 5.
Figure 5.
A, Mean ± SEM performance in acquisition of place conditioning (context/place-cue retrieval) after sham, NAc core, or shell lesions, expressed as number of approaches to CS+ and CS−. B, Conditioned place preference (CPP) performance expressed as total time spent in each of the chamber (within a 5 min session) of sham controls, NAc core, and shell lesion groups.
Figure 6.
Figure 6.
Mean ± SEM performance of sham-operated controls and NAc core or shell lesion groups in discrete cue conditioning. A, Acquisition expressed as number of approaches to the CS within 15 s (correct trial). B, Locomotor activity. C, General nose-poke activity.
Figure 7.
Figure 7.
A, B, Mean ± SEM performance in the acquisition of place conditioning (context/place-cue retrieval) after disconnection sham, unilateral NAc shell, or HPC or disconnection lesions, expressed as number of approaches to CS+ and CS− (A) or expressed as a difference score [number of approaches to CS+ − number of approaches to CS− (B)].
Figure 8.
Figure 8.
Conditioned place preference (CPP) performance expressed as the total time spent in each of the chamber (within 5 min) of disconnection sham controls, unilateral NAc shell, or HPC and disconnection lesion groups.
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