Engaged decision-makers align spontaneous movements to stereotyped task demands.

Neural activity during sensory-guided decision-making is strongly modulated by animal movements. Although the impact of movements on neural activity is now well-documented, the relationship between these movements and behavioral performance remains unclear. To understand this relationship, we first tested whether the magnitude of animal movements (assessed with posture analysis of 28 individual body parts) was correlated with performance on a perceptual decision-making task. No strong relationship was present, suggesting that task performance is not affected by the magnitude of movements. We then tested if performance instead depends on movement timing and trajectory. We partitioned the movements into two groups: task-aligned movements that were well predicted by task events (such as the onset of the sensory stimulus or choice) and task independent movement (TIM) that occurred independently of task events. TIM had a reliable, inverse correlation with performance in head-restrained mice and freely moving rats. This argues that certain movements, defined by their timing and trajectories relative to task events, might indicate periods of engagement or disengagement in the task. To confirm this, we compared TIM to the latent behavioral states recovered by a hidden Markov model with Bernoulli generalized linear model observations (GLM-HMM) and found these, again, to be inversely correlated. Finally, we examined the impact of these behavioral states on neural activity measured with widefield calcium imaging. The engaged state was associated with widespread increased activity, particularly during the delay period. However, a linear encoding model could account for more overall variance in neural activity in the disengaged state. Our analyses demonstrate that this is likely because uninstructed movements had a greater impact on neural activity during disengagement. Taken together, these findings suggest that TIM is informative about the internal state of engagement, and that movements and state together have a major impact on neural activity.

Divergent projections of the prelimbic cortex bidirectionally regulate active avoidance.

The prefrontal cortex (PFC) integrates incoming information to guide our actions. When motivation for food-seeking competes with avoidance of danger, the PFC likely plays a role in selecting the optimal choice. In platform-mediated active avoidance, rats avoid a tone-signaled footshock by stepping onto a nearby platform, delaying access to sucrose pellets. This avoidance requires prelimbic (PL) PFC, basolateral amygdala (BLA), and ventral striatum (VS). We previously showed that inhibitory tone responses of PL neurons correlate with avoidability of shock (Diehl et al., 2018). Here, we optogenetically modulated PL terminals in VS and BLA to identify PL outputs regulating avoidance. Photoactivating PL-VS projections reduced avoidance, whereas photoactivating PL-BLA projections increased avoidance. Moreover, photosilencing PL-BLA or BLA-VS projections reduced avoidance, suggesting that VS receives opposing inputs from PL and BLA. Bidirectional modulation of avoidance by PL projections to VS and BLA enables the animal to make appropriate decisions when faced with competing drives.