Dynamic encoding of stimulus-reward associations by network activity
in the striatum

stimuli. When stimulus-reward associations are changed, rats quickly switch their behavior and attempt to collect rewards to newly rewarded stimuli. My graduate student, Eyal Kimchi, and I have examined changes in neuronal activity in the dorsal (caudate) and ventral (accumbens) portions of the medial striatum during this task. Changing the reward value of a stimulus leads to three specific effects on neuronal activity. First, approximately 20% of neurons exhibit almost immediate changes in firing rate when rats respond to newly rewarded stimuli. These neurons are distributed throughout the dorsal-to-ventral extent of the medial striatum. Second, local field potentials (LFPs) exhibit enhanced movement-related potentials, especially in the dorsal striatum, and altered power in the theta band (5-10 Hz) when rats respond to newly rewarded stimuli. Third, many striatal neurons fire in phase with ongoing LFP oscillations, with more than half of all neurons coupled to theta oscillations. Spike-field coupling is reduced during the reaction time epoch when stimuli become rewarded. This effect is independent of effects of reward value on reaction times, which are shorter to rewarded stimuli, and is not correlated with neuronal firing rates. Changes in spike-field coupling are observed for neurons that are sensitive to reward value, for neurons that are insensitive to reward value, and for neurons that are not modulated during the reaction time epoch. That is, changes in spike-field coupling occur across a much larger proportion of neurons than would expected based on firing rate measures of stimulus reward value. The association between a stimulus and a reward is therefore encoded not only by the activity of reward-sensitive striatal neurons, but also by the activity ofthe striatal network.