Tightly-coupled inhibitory and excitatory functional networks in the early visual cortex

Abstract

Intracortical inhibition plays a critical role in shaping activity patterns in the mature cortex. However, little is known about the structure of inhibition in early development prior to the onset of sensory experience, a time when spontaneous activity exhibits long-range correlations predictive of mature functional networks. Here, using calcium imaging of GABAergic neurons in the early ferret visual cortex, we show that spontaneous activity in inhibitory neurons is already highly organized into distributed modular networks before visual experience. Inhibitory neurons exhibit spatially modular activity with long-range correlations and precise local organization that is in quantitative agreement with excitatory networks. Furthermore, excitatory and inhibitory networks are strongly co-aligned at both millimeter and cellular scales. These results demonstrate a remarkable degree of organization in inhibitory networks early in the developing cortex, providing support for computational models of self-organizing networks and suggesting a mechanism for the emergence of distributed functional networks during development.

Developmental maturation of millimeter-scale functional networks across brain areas

“…Prior work has suggested that in early development, when intracortical horizontal connections are thought to be primarily short-range (Durack and Katz, 1996), recurrent local circuits can give rise to distributed and modular correlations through self-organizing mechanisms (Smith et al, 2018;Mulholland et al, 2024). In such theoretical models (von der Malsburg, 1973;Ernst et al, 2001), this modular structure arises through the interaction of local excitation and lateral inhibition (LE/LI), and predicts a tight coupling of activity in excitatory and inhibitory populations, which has been observed in V1 in early development (Mulholland et al, 2021).…”

“…In such theoretical models (von der Malsburg, 1973;Ernst et al, 2001), this modular structure arises through the interaction of local excitation and lateral inhibition (LE/LI), and predicts a tight coupling of activity in excitatory and inhibitory populations, which has been observed in V1 in early development (Mulholland et al, 2021). Such LE/LI mechanisms appear to be engaged in early V1 where unstructured optogenetic activation gives rise to modular cortical activity (Mulholland et al, 2024). It is possible that a similar mechanism may operate in early development in other cortical regions, although this remains to be tested.…”