Rapid Whisker Movements in Sleeping Newborn Rats

Abstract

Summary Spontaneous activity in the sensory periphery drives infant brain activity and is thought to contribute to the formation of retinotopic and somatotopic maps [1–3]. In infant rats during active (or REM) sleep, brainstem-generated spontaneous activity triggers hundreds of thousands of skeletal muscle twitches each day [4]; sensory feedback arising from the resulting limb movements is a primary activator of forebrain activity, including spindle bursts in somatosensory cortex [1]. The rodent whisker system, with its precise isomorphic mapping of individual whiskers to discrete brain areas, has been a key contributor to our understanding of somatotopic maps and developmental plasticity [5–7]. However, in contrast with other sensory systems—and even though whisker movements are controlled by dedicated skeletal muscles [8, 9]—spontaneous whisker activity has not been entertained as a contributing factor to the development of this system [10]. Here we report in 3- to 6-day-old rats that whiskers twitch rapidly and asynchronously during active sleep. In addition, neurons in whisker thalamus exhibit bursts of activity that are tightly associated with twitches, but occur infrequently during waking. Finally, we observed barrel-specific cortical activity during periods of twitching. This is the first report of self-generated, sleep-related twitches in the developing whisker system, a sensorimotor system that is unique for the precision with which it can be experimentally manipulated. Therefore, the discovery of whisker twitching will allow us to attain a fuller understanding of the contributions of peripheral sensory activity to somatosensory integration and plasticity in the developing nervous system [11–13].

Self-Generated Movements with “Unexpected” Sensory Consequences

“…Across all pups, there was a significant increase in mean rates of spindle bursts ( t 10 = 9.2, P < 0.01) and mean unit firing rates ( t 16 = 3.2, P < 0.01, n = 17 units, 1–2 units per pup) during sleep (Figure 1D). Moreover, LFP power and unit activity increased significantly after twitches with a latency of at least 100–125 ms (Figure 1E), consistent with previous reports of twitch-related reafference in cerebral cortex [21, 22]. Finally, these results were replicated in P4 and P12 rats, demonstrating the stability of the effect across early development (Figure S1).…”

“…The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23].…”

Avian Versus Mammalian Sleep: the Fruits of Comparing Apples and Oranges

“…Although additional species need to be studied, the results from owls suggest that a high amount of REM sleep early in life is another fundamental feature of sleep shared by mammals and birds. As proposed for mammals [52,53], REM sleep may therefore also play a role in brain development in birds.…”

Resonance properties of different neuronal populations in the immature mouse neocortex

“…In the whisker system, gamma and spindle bursts modulate both thalamic-cortico and cortico-thalamic network loops (Minlebaev et al, 2011;Yang et al, 2012). In addition, the precise topographic and functional columnar organization in barrel cortex also needs the localized gamma and spindle bursts in neonatal vibrissal S1 (Yang et al, 2012) induced by the spontaneous whisker movements (Tiriac et al, 2012). In the visual system, the patterned spontaneous retinal waves not only contribute to the retinotopic map refinement in the superior colliculus (McLaughlin et al, 2003;Chandrasekaran et al, 2005), but also trigger spindle bursts required for the development of precise maps in V1 (Cang et al, 2005).…”