Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex

Cortical development is an activity-dependent process [1–3]. Regarding the role of activity in the developing somatosensory cortex, one persistent debate concerns the importance of sensory feedback from self-generated movements. Specifically, recent studies claim that cortical activity is generated intrinsically, independent of movement [3, 4]. However, other studies claim that behavioral state moderates the relationship between movement and cortical activity [5–7]. Thus, perhaps inattention to behavioral state leads to failures to detect movement-driven activity [8]. Here, we resolve this issue by associating local field activity (i.e., spindle bursts) and unit activity in the barrel cortex of 5-day-old rats with whisker movements during wake and myoclonic twitches of the whiskers during active (REM) sleep. Barrel activity increased significantly within 500 ms of whisker movements, especially after twitches. Also, higher-amplitude movements were more likely to trigger barrel activity; when we controlled for movement amplitude, barrel activity was again greater after a twitch than a wake movement. We then inverted the analysis to assess the likelihood that increases in barrel activity were preceded within 500 ms by whisker movements: at least 55% of barrel activity was attributable to sensory feedback from whisker movements. Finally, when periods with and without movement were compared, 70%–75% of barrel activity was movement related. These results confirm the importance of sensory feedback from movements in driving activity in sensorimotor cortex and underscore the necessity of monitoring sleep-wake states to ensure accurate assessments of the contributions of the sensory periphery to activity in developing somatosensory cortex. [Display omitted] •In newborn rats, self-generated whisker movements trigger barrel cortex activity•Larger whisker movements are more likely to trigger responses in barrel cortex•Movement-related cortical activity occurs more often during active sleep than wake•When pups don’t move at all, there is a 3-fold reduction in cortical activity Some researchers have questioned whether sensory feedback from movements drives activity in developing somatosensory cortex. On the contrary, using infant rats, Dooley et al. establish that activity in barrel cortex depends critically on sensory feedback from whisker movements, particularly during active sleep.