Abstract
Disruptions in attention, salience and increased distractibility are implicated in multiple psychiatric conditions. The ventral tegmental area (VTA) is a potential site for converging information about external stimuli and internal states to be integrated and guide adaptive behaviours. Given the dual role of dopamine signals in both driving ongoing behaviours (e.g., feeding) and monitoring salient environmental stimuli, understanding the interaction between these functions is crucial. Here, we investigate VTA neuronal activity during distraction from ongoing feeding. We developed a task to assess distraction exploiting self‐paced licking in rats. Rats trained to lick for saccharin were given a distraction test, in which three consecutive licks within 1 s triggered a random distractor (e.g. light and tone stimulus). On each trial they were quantified as distracted or not based on the length of their pauses in licking behaviour. We expressed GCaMP6s in VTA neurons and used fibre photometry to record calcium fluctuations during this task as a proxy for neuronal activity. Distractor stimuli caused rats to interrupt their consumption of saccharin, a behavioural effect which quickly habituated with repeat testing. VTA neural activity showed consistent increases to distractor presentations and, furthermore, these responses were greater on distracted trials compared to non‐distracted trials. Interestingly, neural responses show a slower habituation than behaviour with consistent VTA responses seen to distractors even after they are no longer distracting. These data highlight the complex role of the VTA in maintaining ongoing appetitive and consummatory behaviours while also monitoring the environment for salient stimuli.
Highlights
To operate effectively in an unpredictable world it is essential for animals to learn to pursue rewards and avoid potential threats and punishments
When all trials were included in the receiver-operator characteristic (ROC) analysis we found no difference in the response to distractors between the distraction and habituation day in any time bin
We find that distracting stimuli, as predicted, cause rats to interrupt their licking and that this behavioural effect habituates such that the stimuli are less likely to distract rats on the second day they are presented
Summary
To operate effectively in an unpredictable world it is essential for animals to learn to pursue rewards and avoid potential threats and punishments. Promoting flexible approach behaviours involves rapid assimilation of external stimuli, at times from multiple modalities, and decision making based on probabilities of opportunity, calculations of cost and effort as well as balancing ongoing behaviours with possible future rewards from new opportunities. Traits such as hyper-vigilance, inappropriate allocation of attention, disrupted novelty detection and increased distraction in humans are hallmarks of several psychiatric diseases including schizophrenia, post-traumatic stress disorder, addiction and anxiety disorders (WintonBrown et al, 2014). We predict that neural activity in VTA will reflect aspects of the ongoing licking behaviour as well as responding to distracting stimuli and, importantly, that whether an animal is distracted or not will be reflected in the neural activity evoked by the stimulus
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