Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Abstract

Ocular dominance plasticity in the developing primary visual cortex is initiated by monocular deprivation (MD) and consolidated during subsequent sleep. To clarify how visual experience and sleep affect neuronal activity and plasticity, we continuously recorded extragranular visual cortex fast-spiking (FS) interneurons and putative principal (i.e., excitatory) neurons in freely behaving cats across periods of waking MD and post-MD sleep. Consistent with previous reports in mice, MD induces two related changes in FS interneurons: a response shift in favor of the closed eye and depression of firing. Spike-timing-dependent depression of open-eye-biased principal neuron inputs to FS interneurons may mediate these effects. During post-MD nonrapid eye movement sleep, principal neuron firing increases and becomes more phase-locked to slow wave and spindle oscillations. Ocular dominance (OD) shifts in favor of open-eye stimulation-evident only after post-MD sleep -are proportional to MD-induced changes in FS interneuron activity and to subsequent sleep-associated changes in principal neuron activity. OD shifts are greatest in principal neurons that fire 40-300 ms after neighboring FS interneurons during post-MD slow waves. Based on these data, we propose that MD-induced changes in FS interneurons play an instructive role in ocular dominance plasticity, causing disinhibition among open-eye-biased principal neurons, which drive plasticity throughout the visual cortex during subsequent sleep.period shifts neuronal responses in primary visual cortex in favor of open-eye stimulation. Sleep is essential for consolidating ocular dominance plasticity (ODP) in cat visual cortex (1, 2). Specifically, post-MD sleep is required to potentiate open-eye responses in cortical neurons-a process mediated via intracellular pathways involved in long-term potentiation of glutamatergic synapses (1, 3). However, the changes in network activity (during waking experience and subsequent sleep) that mediate ODP remain unknown.One long-standing hypothesis is that ODP is gated by the balance of excitation and inhibition in the visual cortex during the critical period. This idea is supported by findings that ODP is enhanced either by increasing GABAergic neurotransmission before the critical period (4) or by reducing GABA signaling after the critical period (5-8). It has been suggested that, during the critical period, MD itself alters the balance of excitation and feedback inhibition within the visual cortex by depressing the activity of fast-spiking (FS) interneurons (9, 10). In support of this idea, ODP is first detectable in the extragranular cortical layers [i.e., 2/3, 5, and 6 (11)], where depression of FS interneuron activity has been reported after brief MD. These layers are characterized by abundant reciprocal intralaminar connections between FS interneurons and pyramidal neurons (12, 13). In contrast, in layer 4, where ODP is initially weak or absent (11), connections between FS interneurons and pyramidal neurons can be strengthened by MD ...

Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity

“…sleep | vision | thalamocortical | plasticity | coherence C onverging behavioral (1), biochemical (2-4), neuroanatomical (5), and electrophysiological (2,(6)(7)(8) evidence supports the idea that following novel sensory experiences, sleep can promote cortical plasticity. The sleep-dependent mechanisms driving these changes have remained elusive.…”

“…The sleep-dependent mechanisms driving these changes have remained elusive. Sleep-associated changes in network activity (1,6,7,9,10), neuromodulator tone (11), transcription (4), translation (4), and protein phosphorylation (2,3) have all been correlated with cortical plasticity following novel experiences (12). In recent years, neuroscientists have speculated that the high-amplitude, low-frequency thalamocortical oscillations that characterize nonrapid eye movement (NREM) sleep play a critical role in promoting sensory cortical plasticity and learning (12).…”

Do infants retain the statistics of a statistical learning experience? Insights from a developmental cognitive neuroscience perspective

“…Downscaling is thought to occur monotonically according to the strength of the association so that stronger associations (with greater buildup of synaptic energy) should survive downscaling to a greater extent than weaker ones. Sleep consolidation through cortical long-term potentiation is a competing possibility [83]. Although we would expect stronger associations to consolidate to a greater degree than weaker ones, by this view, we would not expect robust consolidation given the immaturity of cortical networks in early development.…”

Rapid Developmental Emergence of Stable Depolarization during Wakefulness by Inhibitory Balancing of Cortical Network Excitability

“…The idea that active state development is a limiting step in cortical development clarifies and unites a number of disparate observations of human and animal EEG development. These include the observations that human sleep/ wake EEG patterns are reorganized around term (André et al, 2010;Scher, 2011), that EEG infra-slow activities (Tolonen et al, 2007;Colonnese and Khazipov, 2010) and sensory responses decrease during development, and that neural desynchronization occurs in S1 (Golshani et al, 2009) andV1 (Rochefort et al, 2009) during these early postnatal ages. Directly measuring intracellular V m in vivo produced multiple results that could not have been predicted from previous extracellular and current recordings.…”

“…Electrophysiological studies in both preterm infants and animal models suggest that a minimal component of cortical active states or desynchronization, continuous activity strongly modulated by sleep/wake states, is absent during the first stage and develops during the second. The transition to the second stage occurs at ages equivalent to the human perinatal period (Dreyfus-Brisac and Monod, 1965;Jouvet-Mounier et al, 1970;Gramsbergen, 1976;Frank and Heller, 1997;Golshani et al, 2009;Rochefort et al, 2009;André et al, 2010;Seelke and Blumberg, 2010;Berkes et al, 2011). Infants show signs of alert processing and visual recognition at birth (Colombo, 2001;Daw, 2006), suggesting that basic network mechanisms of alertness/wakefulness are already in place by birth.…”