The Nature of the Sensory Input to the Neonatal Rat Barrel Cortex

Abstract

Sensory input plays critical roles in the development of the somatosensory cortex during the neonatal period. This early sensory input may involve: (1) stimulation arising from passive interactions with the mother and littermates and (2) sensory feedback arising from spontaneous infant movements. The relative contributions of these mechanisms under natural conditions remain largely unknown, however. Here, we show that, in the whisker-related barrel cortex of neonatal rats, spontaneous whisker movements and passive stimulation by the littermates cooperate, with comparable efficiency, in driving cortical activity. Both tactile signals arising from the littermate's movements under conditions simulating the littermates' position in the litter, and spontaneous whisker movements efficiently triggered bursts of activity in barrel cortex. Yet, whisker movements with touch were more efficient than free movements. Comparison of the various experimental conditions mimicking the natural environment showed that tactile signals arising from the whisker movements with touch and stimulation by the littermates, support: (1) a twofold higher level of cortical activity than in the isolated animal, and (2) a threefold higher level of activity than in the deafferented animal after the infraorbital nerve cut. Together, these results indicate that endogenous (self-generated movements) and exogenous (stimulation by the littermates) mechanisms cooperate in driving cortical activity in newborn rats and point to the importance of the environment in shaping cortical activity during the neonatal period.

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

“…Specifically, in infant rats before postnatal day (P) 11, whereas sensory feedback from limb movements during wake only weakly activates sensorimotor cortex, sensory feedback from limb twitches during active sleep triggers strong cortical responses [5][6][7]. However, in many studies of activity in developing somatosensory cortex, either behavioral state was not measured [4,9,10] or the subjects were anesthetized [11][12][13]. It is plausible, then, that by ignoring behavioral state, we underestimate the importance of sensory feedback from selfgenerated movements for driving early neural activity.To address this issue directly, we recorded whisker movements during active sleep (AS) and wake (W) in P5 rats while recording extracellular activity in the C row of barrel cortex.…”

Active Sleep Promotes Functional Connectivity in Developing Sensorimotor Networks

“…Twitch-following somatotopic [12,16,48,[76][77][78] Twitch-following somatotopic [79] Primary motor cortex Rat P4-12 Twitch-following somatotopic AS-On…”

“…The study in Ref. [77] also uses voltage-sensitive dye imaging. MUA, multi-unit activity; LFP, local field potential; EEG, electroencephalogram; P, postnatal day; PCA, post-conceptional age (in weeks); CA, cornus amonius; DG, dentate gyrus; Gi, nucleus gigantocellularis; LC, locus coeruleus.…”

“…Based on such studies, one might conclude that the expression of brain rhythms is independent of experience or behavioral state. Within the developing sensorimotor system, however, early neural oscillations are largely triggered by sensory input arising from external stimulation ( exafference ) or sensory feedback arising from self‐generated movements ( reafference ) …”

“…Within the developing sensorimotor system, however, early neural oscillations are largely triggered by sensory input arising from external stimulation (exafference) or sensory feedback arising from self-generated movements (reafference). [9,22] The opportunities for reafferent stimulation in the developing sensorimotor system are not restricted to periods of wakefulness. In the perinatal period when sleep is the predominant behavioral state, myoclonic twitching during active sleep is one of the most abundant of all behaviors.…”