Tightly coupled inhibitory and excitatory functional networks in the developing primary visual cortex.

Haleigh N Mulholland,Matthias Kaschube,Bettina Hein,Gordon B Smith

doi:10.7554/elife.72456

Haleigh N Mulholland, Matthias Kaschube + Show 2 more

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https://doi.org/10.7554/elife.72456

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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 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.

Highlights

Inhibition is crucial for shaping neural activity and response properties in mature cortex
That correlated excitatory and inhibitory networks exhibit a similar spatial scale at the cellular level (Figure 6e,f). These results show that excitatory and inhibitory neurons are precisely organized in the early visual cortex into the same spatially structured and locally correlated functional networks
Inhibitory networks exhibit quantitatively similar structure to excitatory networks, which together show precise alignment at both local and global scales in the patterns of correlated spontaneous activity. These findings demonstrate the presence of tightly-coupled excitatory and inhibitory functional networks in the early visual cortex

Summary

Introduction

Inhibition is crucial for shaping neural activity and response properties in mature cortex. Recent work in the ferret visual cortex demonstrated that prior to the onset of visual experience, excitatory activity is already highly structured, showing modular and distributed activity with long-range correlations (Smith et al, 2018), reminiscent of the columnar stimulus-evoked activity found in the mature cortex (Hubel and Wiesel, 1968; Blasdel and Salama, 1986; Weliky, Bosking and Fitzpatrick, 1996; Issa, Trepel and Stryker, 2000; Kara and Boyd, 2009; Smith, Whitney and Fitzpatrick, 2015) These early correlated networks are not abolished when silencing feedforward activity and predict future visually-evoked responses (Smith et al, 2018), suggesting a key role for early spontaneous activity in the development of mature cortical networks. Top row: Excitation is known to be might be organized and modular, but poorly aligned with highly modular and spatially structured

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