![]() Nevertheless, both spontaneous behaviour and structured tasks demand that animals choose actions on an ongoing basis from a distribution of possibilities, suggesting that dopamine may influence the continuous assembly of naturalistic sequences through mechanisms similar to those used to support goal-driven action selection in response to rewards. ![]() By contrast, during structured tasks in which animals seek explicit and often cued rewards, phasic dopamine clearly conveys information related to reward and reward-prediction errors, reinforces reward-associated actions, and influences the choices made between alternative actions 20, 21, 22, 23, 24, 25.ĭopamine may have distinct roles during spontaneous and task-structured behaviours, given the many ways in which they differ for example, spontaneous behaviours generally exhibit a greater variety of expressed behavioural modules, include more complex behavioural sequences, and tend to emphasize self-initiated movements associated with active sensing 2, 4, 26. ![]() Although dopamine is thought to motivate spontaneous behaviour and to influence the vigour with which actions are expressed, evidence is mixed as to whether phasic dopamine transients are permissive or causal for movements, whether dopamine rises or falls when animals initiate a movement, and whether dopamine fluctuations specify movement kinematics in freely behaving animals 6, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19. Yet we know little about the precise relationship between dopamine and behaviour when animals freely explore an environment. Given that the loss of dopaminergic neurons from the substantia nigra pars compacta (SNc) causes diffuse deficits in action initiation and sequencing, it is likely that the neuromodulator dopamine influences the architecture of spontaneous behaviour 6, 7, 8. However, it remains unclear how the brain regulates the expression of individual behavioural modules at any given moment, or how it dynamically composes these modules into the fluid behaviours observed when animals act of their own volition in the absence of experimental restraint, task structure or exogenous reward. Many well-studied laboratory behaviours-including chemotaxis, grooming, prey seeking, courtship, birdsong and exploratory locomotion-are similarly characterized by modularity and predictability 2, 3, 4, 5. Ethologists have long argued that the self-motivated behaviour of animals in the wild is flexibly built from modular components that are linked together over time in a predictable yet probabilistic manner 1. ![]() Spontaneous behaviour exhibits structure. Together, these findings suggest a model in which the same circuits and computations that govern action choices in structured tasks have a key role in sculpting the content of unconstrained, high-dimensional, spontaneous behaviour. Consistent with the possibility that DLS dopamine fluctuations act as a teaching signal, mice build sequences during exploration as if to maximize dopamine. Although the reinforcing effects of optogenetic DLS dopamine manipulations vary across behavioural modules and individual mice, these differences are well predicted by observed variation in the relationships between endogenous dopamine and module use. Photometric recordings and calibrated closed-loop optogenetic manipulations during open field behaviour demonstrate that DLS dopamine fluctuations increase sequence variation over seconds, reinforce the use of associated behavioural modules over minutes, and modulate the vigour with which modules are expressed, without directly influencing movement initiation or moment-to-moment kinematics. Here we show that dopamine systematically fluctuates in the dorsolateral striatum (DLS) as mice spontaneously express sub-second behavioural modules, despite the absence of task structure, sensory cues or exogenous reward. However, the neural mechanisms that guide the composition of naturalistic, self-motivated behaviour remain unknown. Spontaneous animal behaviour is built from action modules that are concatenated by the brain into sequences 1, 2.
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