Input-independent homeostasis of developing thalamocortical activity

Abstract

The isocortex of all mammals studied to date shows a progressive increase in the amount and continuity of background activity during early development. In humans the transition from a discontinuous (mostly silent, intermittently bursting) cortex to one that is continuously active is complete soon after birth and is a critical prognostic indicator in newborns. In the visual cortex of rodents this switch from discontinuous to continuous background activity occurs rapidly during the two days before eye-opening, driven by activity changes in relay thalamus. The factors that regulate the timing of continuity development, which enables mature visual processing, are unknown. Here we test the role of the retina, the primary input, in the development of continuous spontaneous activity in the visual system of mice using depth electrode recordings of cortical activity from enucleated mice in vivo. Bilateral enucleation at postnatal day (P)6, one week prior to the onset of continuous activity, acutely silences cortex, yet firing rates and early oscillations return to normal within two days and show a normal developmental trajectory through P12. Enucleated animals showed differences in silent period duration and continuity on P13 that resolved on P16, and an increase in low frequency power that did not. Our results show that the timing of cortical activity development is not determined by the major driving input to the system. Rather, homeostatic mechanisms in thalamocortex regulate firing rates and continuity even across periods of rapid maturation.

Activity in developing prefrontal cortex is shaped by sleep and sensory experience

“…Also, the transition from discontinuous cortical activity at P8 to continuous activity at P12 is evident in all three areas, as described previously in primary somatosensory, motor, and visual cortex (Golshani et al, 2009;Rochefort et al, 2009;Van Der Bourg et al, 2017;Glanz et al, 2021;Riyahi et al, 2021).…”

“…As expected (Dooley et al, 2021; Glanz et al, 2021; Gómez et al, 2021), pups spent more time in AS than wake at P8 (AS: 57.7 ± 2.5%; wake: 30.9 ± 1.9%) and P12 (AS: 44.0 ± 3.6%; wake: 39.3 ± 3.5%). Also, the transition from discontinuous cortical activity at P8 to continuous activity at P12 is evident in all three areas, as described previously in primary somatosensory, motor, and visual cortex (Golshani et al, 2009; Rochefort et al, 2009; Van Der Bourg et al, 2017; Glanz et al, 2021; Riyahi et al, 2021).…”

Sensory Coding of Limb Kinematics in Motor Cortex across a Key Developmental Transition

“…6A). Neural activity in S1 (Golshani et al, 2009;van der Bourg et al, 2017) and primary visual cortex (V1; Rochefort et al, 2009;Riyahi et al, 2021) is similarly discontinuous at this age. It has been hypothesized that discontinuous activity helps to maximize the detection of spontaneous peripheral activity (Colonnese and Phillips, 2018), thereby aiding in the activity-dependent development of sensory networks (Katz and Shatz, 1996;Blankenship and Feller, 2010;Ackman et al, 2012).…”

“…At P12, however, correlated activity disappears as background activity, sparsity (a measure of the uniform distribution of action potentials), and entropy (a measure of informational capacity) increase. Such sparsification of cortical activity in M1 also occurs at approximately P12 in S1 (Golshani et al, 2009;van der Bourg et al, 2017) and V1 (Rochefort et al, 2009;Riyahi et al, 2021). Sparsification of cortical activity is timed contemporaneously with the sudden emergence of local cortical inhibition (Ben-Ari et al, 2007;Colonnese, 2014;Dooley and Blumberg, 2018).…”

Spontaneous thalamic activity modulates the cortical innervation of the primary visual nucleus of the thalamus

“…Eye-opening occurs in mice at around P13, an event that is crucial for the final maturation and refinement of the visual system (Rochefort et al, 2009; Ko et al, 2013; Riyahi et al, 2021). As the decreased corticothalamic innervation of the dLGN observed at P9 is rescued by P30, we assessed whether eye-opening might play a role in this recovery.…”