Retinal Waves Trigger Spindle Bursts in the Neonatal Rat Visual Cortex

Abstract

During visual system development, the light-insensitive retina spontaneously generates waves of activity, which are transmitted to the lateral geniculate nucleus. The crucial question is whether retinal waves are further transmitted to the cortex and influence the early cortical patterns of activity. Using simultaneous recordings from the rat retina and visual cortex during the first postnatal week in vivo, we found that spontaneous retinal bursts are correlated with spindle bursts (intermittent network bursts associated with spindle-shape field oscillations) in the contralateral visual cortex (V1). V1 spindle bursts could be evoked by electrical stimulation of the optic nerve. Intraocular injection of forskolin, which augments retinal waves, increased the occurrence of V1 spindle bursts. Blocking propagation of retinal activity, or removal of the retina reduced the frequency, but did not completely eliminate the cortical spindle bursts. These results indicate that spontaneous retinal waves are transmitted to the visual cortex and trigger endogenous spindle bursts. We propose that the interaction between retinal waves and spindle bursts contributes to the development of visual pathways to the cortex.

GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo

“…4h). In summary, the electrophysiological characteristics of Ca 2 þ clusters agree well with those of previously reported spindle bursts in the visual cortex of neonatal rats [50][51][52] . Although the aforementioned measurements were acquired through the intact dura after surgical removal of the overlying bone, virtually identical Ca 2 þ cluster activity was observed through the intact skull (n ¼ 3 mice; Supplementary Fig.…”

“…At present, it is unclear which factors underlie this discrepancy. Certainly, slow active chloride uptake in immature neurons 62 in conjunction with a higher chloride conductance in vivo versus in vitro, for example, due to synaptic 50 or extrasynaptic GABA A R activation, represents a potential candidate 25 . Whether traumatic injury might affect results obtained from in vitro preparations is currently highly debated 28,44 .…”

Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual CortexIn Vivo

“…We also tested the effect of BFn stimulation in newborn rats. None of the three investigated P0 -P1 pups displayed spindle bursts in control conditions (see also Hanganu et al, 2006) or in response to BFn-stimulation. Because mAChRs agonists evoke beta oscillations in the P0 -P1 neocortex in vitro (Dupont et al, 2006), the lack in the effect of BFn stimulation may reflect the immaturity of the cholinergic BFn input to neocortex at birth.…”

“…Previously, we identified similar oscillatory activity patterns in the neonatal [postnatal day 2 (P2)-P6] visual cortex in vivo . These self-organized oscillations, termed as spindle bursts, are driven by retinal waves (Khazipov et al, 2004;Hanganu et al, 2006) and are likely to be subject to intense modulation (Luhmann and . However, to which extent the cholinergic drive interacts with the early network activity in vivo remains widely unknown.…”

Interaction between neocortical and hippocampal networks via slow oscillations

“…The emerging thalamic spindles are transferred to the neocortex via topographic thalamo-cortical projections, and the spatially contiguous or distinct thalamic oscillations are synchronized by cortico-thalamic feedback (Kim et al, 1995;. Thalamo-cortical spindles represent the first organized pattern in the neocortex in newborn rats and pre-term human babies (Khazipov et al, 2004;Hanganu et al, 2006;Milh et al, 2006), although these early spindles are confined spatially. After the establishment of longrange cortico-cortical connections, spindles typically occur virtually synchronously across wide areas of the thalamus and cortex (Verzeano and Negishi, 1960;Bal et al, 2000).…”