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Abstract Processing sensory information, generating perceptions, and shaping behavior engages neural networks in brain areas with highly varied representations, ranging from unimodal sensory cortices to higher-order association areas. In early development, these areas share a common distributed and modular functional organization, but it is not known whether this undergoes a common developmental trajectory, or whether such organization persists only in some brain areas. Here, we examine the development of network organization across diverse cortical regions in ferrets using in vivo wide field calcium imaging of spontaneous activity. In both primary sensory (visual, auditory, and somatosensory) and higher order association (prefrontal and posterior parietal) areas, spontaneous activity remained significantly modular with pronounced millimeter-scale correlations over a 3-wk period spanning eye opening and the transition to externally-driven sensory activity. Over this period, cortical areas exhibited a roughly similar set of developmental changes, along with area-specific differences. Modularity and long-range correlation strength generally decreased with age, along with increases in the dimensionality of activity, although these effects were not uniform across all brain areas. These results indicate an interplay of area-specific factors with a conserved developmental program that maintains modular functional networks, suggesting modular organization may be involved in functional representations in diverse brain areas. 

Abstract During development, cortical activity is organized into distributed modular patterns that are a precursor of the mature columnar functional architecture. Theoretically, such structured neural activity can emerge dynamically from local synaptic interactions through a recurrent network with effective local excitation with lateral inhibition (LE/LI) connectivity. Utilizing simultaneous widefield calcium imaging and optogenetics in juvenile ferret cortex prior to eye opening, we directly test several critical predictions of an LE/LI mechanism. We show that cortical networks transform uniform stimulations into diverse modular patterns exhibiting a characteristic spatial wavelength. Moreover, patterned optogenetic stimulation matching this wavelength selectively biases evoked activity patterns, while stimulation with varying wavelengths transforms activity towards this characteristic wavelength, revealing a dynamic compromise between input drive and the network’s intrinsic tendency to organize activity. Furthermore, the structure of early spontaneous cortical activity – which is reflected in the developing representations of visual orientation – strongly overlaps that of uniform opto-evoked activity, suggesting a common underlying mechanism as a basis for the formation of orderly columnar maps underlying sensory representations in the brain. 

In order to deal with a complex environment, animals form a diverse range of neural representations that vary across cortical areas, ranging from largely unimodal sensory input to higher-order representations of goals, outcomes, and motivation. The developmental origin of this diversity is currently unclear, as representations could arise through processes that are already area-specific from the earliest developmental stages or alternatively, they could emerge from an initially common functional organization shared across areas. Here, we use spontaneous activity recorded with two-photon and widefield calcium imaging to reveal the functional organization across the early developing cortex in ferrets, a species with a well-characterized columnar organization and modular structure of spontaneous activity in the visual cortex. We find that in animals 7 to 14 d prior to eye-opening and ear canal opening, spontaneous activity in both sensory areas (auditory and somatosensory cortex, A1 and S1, respectively), and association areas (posterior parietal and prefrontal cortex, PPC and PFC, respectively) showed an organized and modular structure that is highly similar to the organization in V1. In all cortical areas, this modular activity was distributed across the cortical surface, forming functional networks that exhibit millimeter-scale correlations. Moreover, this modular structure was evident in highly coherent spontaneous activity at the cellular level, with strong correlations among local populations of neurons apparent in all cortical areas examined. Together, our results demonstrate a common distributed and modular organization across the cortex during early development, suggesting that diverse cortical representations develop initially according to similar design principles.