Homeostasis of neuronal avalanches during postnatal cortex development in vitro

Abstract

Cortical networks in vivo and in vitro are spontaneously active in the absence of inputs, generating highly variable bursts of neuronal activity separated by up to seconds of quiescence. Previous measurements in adult rat cortex revealed an intriguing underlying organization of these dynamics, termed neuronal avalanches, which is indicative of a critical network state. Here we demonstrate that neuronal avalanches persist throughout development in cortical slice cultures from newborn rats. More specifically, we find that in spite of large variations of average rate in activity, spontaneous bursts occur with power-law distributed sizes (exponent -1.5) and a critical branching parameter close to 1. Our findings suggest that cortical networks homeostatically regulate a critical state during postnatal maturation.

Spontaneous cortical activity in awake monkeys composed of neuronal avalanches

“…1C as well as the power law in nLFP cluster sizes is only present in more superficial layers of the cortex demonstrating layer specificity of the organization (Fig. S4), in line with the localization of neuronal avalanches to superficial layers in the acute slice (16), slice culture (17), and anesthetized rat (15).…”

“…Instead, this property of spontaneous activity emerges when superficial layers of cortex first differentiate from the cortical plate during development (15). Given the dependence of neuronal avalanches on the balance of fast synaptic excitation and inhibition and the neuromodulator dopamine (13,(15)(16)(17), it seems clear that these properties arise from the specific organization of cortical circuitry.…”

“…Thus, given a burst of size s, a burst double that size will occur 2 ␣ times less often, independent of s. More generally, given synchronized activity bursts of sizes s and k ⅐ s (where k is a constant), there will always be a fixed ratio k ␣ between the corresponding probabilities of occurrence. This scaleinvariant dynamics has several key properties: (i) it requires balanced excitatory and inhibitory synaptic transmission (13,15,16); (ii) it arises in vitro and in vivo when superficial layers form during development (15); and (iii) it is maintained over many weeks in the isolated cortex in the absence of input (17), suggesting that the dynamics is an intrinsic property of the cortex. Importantly, neuronal avalanches resemble the dynamics observed in other systems at the critical point between an ordered and disordered dynamics, commonly referred to as the critical state (18)(19)(20).…”

Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3

“…Critical state dynamics allows local events to percolate through the system: although the most likely event in the system is local, i.e., of relatively small size, large events that engage many sites cannot be ignored. Such an organization of cortical activity, which is regulated homeostatically (42), differs profoundly from disinhibited activity, where most events are either small and local or very large and engage most of the network resulting in bimodal event size distributions (18). Neuronal modeling suggests that networks in a critical state optimize information transfer and the dynamical range of inputoutput processing (18,43,44), increase speed and complexity of neuronal pattern formation (45,46), and allow for diverse and precise network synchronization in the absence of epilepsy (17,18).…”

“…After the recordings, the brains were fixed in paraformaldehyde, sectioned, and Nissl-stained to reconstruct the electrode locations. Coronal slices from rat somatosensory cortex (350 m thick) and the VTA (500 m thick) were taken from pups (P0 -P2; Sprague-Dawley), placed on a poly-D-lysinecoated 8 ϫ 8 planar MEA (MultiChannelSystems), cocultured, and recorded in standard culture medium (42). Drugs were either applied topically to the cortex surface (in vivo) or bath-applied (in vitro).…”