Peripheral and Central Inputs Shape Network Dynamics in the Developing Visual Cortex In Vivo

Abstract

Spontaneous network activity constitutes a central theme during the development of neuronal circuitry [1, 2]. Before the onset of vision, retinal neurons generate waves of spontaneous activity that are relayed along the ascending visual pathway [3, 4] and shape activity patterns in these regions [5, 6]. The spatiotemporal nature of retinal waves is required to establish precise functional maps in higher visual areas, and their disruption results in enlarged axonal projection areas (e.g., [7-10]). However, how retinal inputs shape network dynamics in the visual cortex on the cellular level is unknown. Using in vivo two-photon calcium imaging, we identified two independently occurring patterns of network activity in the mouse primary visual cortex (V1) before and at the onset of vision. Acute manipulations of spontaneous retinal activity revealed that one type of network activity largely originated in the retina and was characterized by low synchronicity (L-) events. In addition, we identified a type of high synchronicity (H-) events that required gap junction signaling but were independent of retinal input. Moreover, the patterns differed in wave progression and developmental profile. Our data suggest that different activity patterns have complementary functions during the formation of synaptic circuits in the developing visual cortex.

Spontaneous activations follow a common developmental course across primary sensory areas in mouse neocortex

“…across primary sensory areas in vitro and in vivo and during conditions of sensory deprivation (Golshani et al 2009;Rochefort et al 2009;Siegel et al 2012), with the same postnatal time course. The ubiquity and generality of this trajectory suggest a strong, internally mediated mechanism for patterning spontaneous activity during the development of primary sensory neocortical areas, regardless of the sensory experience of the cortical area during this developmental period.…”

“…Previous work in vivo has shown that within layer 2/3 neurons synchronous activity transitions to sparse activity around the time of eye opening at the beginning of the third postnatal week in primary visual cortex (Siegel et al 2012). The timing of this change suggests that sensory input is necessary.…”

Neural progenitors organize in small-world networks to promote cell proliferation

“…Also, grafted neural stem cells exhibit spontaneous Ca 2+ activity that depends on gap junctions (38). Moreover, different patterns of spontaneous activity has been reported in regions of the developing visual cortex (39), and amplitude and frequency of Ca 2+ oscillations were correlated positively with the rate of neuronal migration (25,26). Our findings show that the spontaneous Ca 2+ activities in each cell are not uncorrelated, independent cell signals, but rather highly ordered signaling events creating small-world networks that follow a scalefree topology.…”

Following the ontogeny of retinal waves: pan-retinal recordings of population dynamics in the neonatal mouse

“…Although most studies have been performed in vitro, these findings have also been validated in vivo (Ackman et al 2012;Siegel et al 2012). The spatiotemporal features encoded in the waves are hypothesized to provide cues for the establishment of retinal receptive fields (Sernagor et al 2001), as well as for eye-specific ON-OFF pathway segregation and visual map formation in retinal targets (Wong & Oakley, 1996;Wong, 1999;Lee et al 2002;Akrouh & Kerschensteiner, 2013).…”