The effects of reward devaluation on cue-evoked modulation of sucrose seeking and neuronal ensemble plasticity in nucleus accumbens

Animals must learn the relationship between food and the environmental cues that predict their availability for the successful procurement of nutrient sources. These cues can gain powerful control over food seeking, but these cue-evoked behaviours must remain flexible and updated upon changes in internal states such as the perceived desirability of food. Recalling these cue-food associations activate subsets of neurons termed ‘neuronal ensembles’ in motivationally relevant brain areas such as the striatum. However, how neuronal ensembles are recruited and physiologically modified following the update of these learned associations has not fully elucidated. To investigate this, we examined the effects of reward devaluation on ensemble plasticity at the levels of recruitment, excitability, and synaptic physiology in sucrose conditioned Fos-GFP mice that express green fluorescent protein (GFP) in recently activated neurons. Neuronal ensemble activation patterns and their physiology were examined using immunohistochemistry and ex vivo electrophysiology, respectively. First, devaluation via four days of ad libitum sucrose consumption, but not caloric satiation, attenuated the ability of the cue to evoke sucrose seeking. Thus, changes in the hedonic, incentive value of sucrose, and not caloric need drove cue-induced sucrose seeking. Also, devaluation attenuated the cue’s ability to recruit a neuronal ensemble in nucleus accumbens (NAc), but not dorsal striatum. Next, devaluation prevented the cue from recruiting a hyper-excitable, GFP+ ensemble in the NAc, but did not alter the physiology of excitatory synapses on these GFP+ neurons. Our findings provide new insights into how updates in the hedonic value of sucrose critically modulates the flexibility of sucrose seeking and recruitment of ensembles with an altered excitability phenotype in the NAc shell.