Self-generated whisker movements drive state-dependent sensory input to developing barrel cortex

Abstract

<jats:title>S<jats:sc>ummary</jats:sc></jats:title><jats:p>Cortical development is an activity-dependent process [1–3]. Regarding the role of activity in 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.</jats:p>

Early peripheral activity alters nascent subplate circuits in the auditory cortex

“…We here study how peripheral auditory activity shapes ACtx. SPNs are present in all sensory areas, and both the visual and the somatosensory system show early spontaneous or sensorily evoked activity, e.g., driven by vision through closed eyelids or self-generated movements (43)(44)(45)(46). We thus speculate that alterations of these early activity patterns will also affect SPNs in the respective cortices.…”

Delta brushes are not just a hallmark of EEG in human preterm infants

“…These results suggest that self‐generated human fetal movements provide sensory feedback and drive delta brushes in the developing somatosensory cortex, contributing to the formation of cortical body maps 22 . Additionally, whisker movements in newborn rats trigger spindle bursts more often during active sleep than wake time 23 . These results indicate that twitches and rapid eye movements occurring during active sleep are important for cortical activity and early brain development in humans.…”

Stable behavioral state-specific large scale activity patterns in the developing cortex of neonates

“…Thereafter, the isoflurane anesthesia was terminated and the animal was allowed to recover on a warming plate (34°C - 36°C) for at least one hour. This well established (Ackman et al, 2012; Adelsberger et al, 2005; Che et al, 2018; Dooley et al, 2020; Hagihara et al, 2015) protocol provided stable recording conditions with similar ongoing in vivo activity patterns, observed within and across experimental animals (Fig. 2-2).…”