Early Gamma Oscillations Synchronize Developing Thalamus and Cortex

Abstract

During development, formation of topographic maps in sensory cortex requires precise temporal binding in thalamocortical networks. However, the physiological substrate for such synchronization is unknown. We report that early gamma oscillations (EGOs) enable precise spatiotemporal thalamocortical synchronization in the neonatal rat whisker sensory system. Driven by a thalamic gamma oscillator and initially independent of cortical inhibition, EGOs synchronize neurons in a single thalamic barreloid and corresponding cortical barrel and support plasticity at developing thalamocortical synapses. We propose that the multiple replay of sensory input in thalamocortical circuits during EGOs allows thalamic and cortical neurons to be organized into vertical topographic functional units before the development of horizontal binding in adult brain.

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.…”

“…Oscillations in the gamma range of frequencies (30 -40 Hz) also exist every 10 -30 s (Yang et al, 2009;Seelke and Blumberg, 2010), whereas long (40 s) bursts of 20 -30 Hz activity repeat every 20 -30 min (Yang et al, 2009). Bursts of gammarange activity have also been described recently in the developing barrel cortex, under control of excitatory thalamic synapses (Minlebaev et al, 2011). Finally, two recent studies report slow (Ͼ0.1 Hz) oscillations in the developing sensory cortices (Colonnese and Khazipov, 2010;Seelke and Blumberg, 2010).…”

“…Distinct patterns of neural activity are found in different neural systems (Yvert et al, 2004;Crépel et al, 2007;Tritsch et al, 2007;Watt et al, 2009), and, in some cases, the function of these patterns has been determined (Torborg and Feller, 2005;Huberman, 2007;Wu et al, 2010). Distinct patterns of neural activity are present within the developing mammalian cortex as well (Garaschuk et al, 2000;Adelsberger et al, 2005;Dupont et al, 2006;Yang et al, 2009;Colonnese and Khazipov, 2010;Seelke and Blumberg, 2010;Minlebaev et al, 2011). Understanding these patterns is crucial because they may provide a template for future task-related activity by controlling axon growth and synaptogenesis (Allene and Cossart, 2010).…”

“…The majority of research has examined its properties within a single sensory domain, either somatosensory (Milh, 2007;Marcano-Reik and Blumberg, 2008;Yang et al, 2009;Colonnese and Khazipov, 2010;Minlebaev et al, 2011) or visual Colonnese and Khazipov, 2010), and it is generally described as local and immobile (Yang et al, 2009). Nevertheless, dynamic spindle bursts have been reported (Khazipov et al, 2004, their supplemental figures), and they are synchronized between hemispheres (Yang et al, 2009).…”

Long-Term Potentiation in the Neonatal Rat Barrel Cortex In Vivo

“…The FP responses to single-whisker stimulation recorded in newborn rat barrel cortex in vivo consisted of an early gamma activity followed by spindle bursts, as described previously (Minlebaev et al, 2007(Minlebaev et al, , 2011Yang et al, 2009). To analyze activity-dependent modifications of the evoked responses, we quantified the slope of the initial negative-going FP response, which reflects the early activation of the cortex via the whisker-to-barrel cortex pathway.…”