Neural responses prior to licking onset in the striatal matrix compartment in mice

Abstract

Licking is a continuous tongue thrust observed during drinking in rodents and humans and is often studied as an essential tongue movement for feeding and swallowing. The striatum, a component of the basal ganglia, plays a critical role in licking onset; however, it is unclear how the two compartments of the striatum--the matrix and striosomes--contribute to the control of licking onset. In this study, we used male and female transgenic mice that selectively expressed Cre recombinase in matrix or striosome neurons and subjected them to operant conditioning based on licking of a spout, during which neuronal activity in both compartments was measured using fiber photometry. Only matrix neurons showed responses prior to licking onset. In addition, the matrix neural response before licking onset was larger when mice licked a spout ipsilateral to the recording hemisphere of the brain than that observed when licking the contralateral spout. This response was observed similarly in mice conditioned to receive a reward regularly and those conditioned to receive a reward randomly, suggesting that the response was unrelated to whether the reward was predictable or unpredictable. Matrix neural activity was negatively correlated with the number of licks during the water intake behavior following the first lick. These findings suggest that matrix neurons are involved in the preparatory process for licking onset as well as in the regulation of licking frequency during water intake. Significant StatementThis study demonstrated that during the expression of operant conditioning behaviors based on licking, striatal matrix neurons showed responses prior to licking onset. Additionally, these responses were larger when the mouse licked the spout ipsilateral to the brain hemisphere undergoing recording than when a spout in the contralateral direction was licked. This result was also true for mice conditioned using either regular or random reward conditions. Additionally, the number of licks during water ingestion behavior following the initial lick was negatively correlated with matrix neuron activity. These changes in matrix neuron activity are suggested to be involved in the preparatory process for licking onset, independent of reward prediction, and in the regulation of licking frequency during drinking.