Internally Mediated Developmental Desynchronization of Neocortical Network Activity

Abstract

During neocortical development, neurons exhibit highly synchronized patterns of spontaneous activity, with correlated bursts of action potential firing dominating network activity. This early activity is eventually replaced by more sparse and decorrelated firing of cortical neurons, which modeling studies predict is a network state that is better suited for efficient neural coding. The precise time course and mechanisms of this crucial transition in cortical network activity have not been characterized in vivo. We used in vivo two-photon calcium imaging in combination with whole-cell recordings in both unanesthetized and anesthetized mice to monitor how spontaneous activity patterns in ensembles of layer 2/3 neurons of barrel cortex mature during postnatal development. We find that, as early as postnatal day 4, activity is highly synchronous within local clusters of neurons. At the end of the second postnatal week, neocortical networks undergo a transition to a much more desynchronized state that lacks a clear spatial structure. Strikingly, deprivation of sensory input from the periphery had no effect on the time course of this transition. Therefore, developmental desynchronization of spontaneous neuronal activity is a fundamental network transition in the neocortex that appears to be intrinsically generated.

Functional Development of Large-Scale Sensorimotor Cortical Networks in the Brain

“…Self-sustained cortical activity as well as activity evoked by spontaneous muscular movements could also play a role (Khazipov et al, 2004;Price et al, 2006). The neonatal rat cortex and, interestingly, that of the premature human baby exhibit spontaneous activity patterns characterized by spindle-like bursts in the 5-25 Hz frequency range spatially confined to local cortical areas (Khazipov and Luhmann, 2006;Golshani et al, 2009). It has been proposed that these high synchronicity patterns result from intrinsic synaptic properties of excitatory neurons and immature inhibition, and could serve cortical map maturation by strengthening or eliminating synapses between coactive neurons (Voutsinos-Porche et al, 2003;Golshani et al, 2009).…”

“…The neonatal rat cortex and, interestingly, that of the premature human baby exhibit spontaneous activity patterns characterized by spindle-like bursts in the 5-25 Hz frequency range spatially confined to local cortical areas (Khazipov and Luhmann, 2006;Golshani et al, 2009). It has been proposed that these high synchronicity patterns result from intrinsic synaptic properties of excitatory neurons and immature inhibition, and could serve cortical map maturation by strengthening or eliminating synapses between coactive neurons (Voutsinos-Porche et al, 2003;Golshani et al, 2009). In the barrel cortex, the transition from the highly correlated state to the more mature decorrelated state also occurs at the end of the second postnatal week (Golshani et al, 2009).…”

“…It has been proposed that these high synchronicity patterns result from intrinsic synaptic properties of excitatory neurons and immature inhibition, and could serve cortical map maturation by strengthening or eliminating synapses between coactive neurons (Voutsinos-Porche et al, 2003;Golshani et al, 2009). In the barrel cortex, the transition from the highly correlated state to the more mature decorrelated state also occurs at the end of the second postnatal week (Golshani et al, 2009). 2 ) and interpolated CSD contour plots at P10 (n ϭ 4) and P21 (n ϭ 4).…”

Voltage-Sensitive Dye Imaging Reveals Dynamic Spatiotemporal Properties of Cortical Activity after Spontaneous Muscle Twitches in the Newborn Rat

“…The study of correlated neural activity in developing mammalian cortex is currently characterized by a variety of patterns, described in a range of preparations, including cortical slices (Garaschuk et al, 2000;Corlew et al, 2004;Sun and Luhmann, 2007;Allene and Cossart, 2010) and the in vivo intact brain (Khazipov et al, 2004;Adelsberger et al, 2005;Marcano-Reik and Blumberg, 2008;Golshani et al, 2009;Seelke and Blumberg, 2010;Minlebaev et al, 2011). Most relevant to our results are patterns of activity described in vivo.…”

A Role for Silent Synapses in the Development of the Pathway from Layer 2/3 to 5 Pyramidal Cells in the Neocortex

“…Spontaneous activity is evident in many developing neuronal circuits (Blankenship and Feller, 2010) including the neocortex (Garaschuk et al, 2000;Khazipov and Luhmann, 2006;Allène et al, 2008;Golshani et al, 2009). However, there is remarkably little understanding of the development of pathways intrinsic to the neocortex that convey such early activity, with previous studies focusing primarily on subplate neurons (Zhao et al, 2009), the period of sensory awakening in the ferret visual cortex (Dalva and Katz, 1994) or the feedforward pathways in the barrel field of the mouse somatosensory cortex (Bureau et al, 2004;Ashby and Isaac, 2011).…”