Distributed network interactions and their emergence in developing neocortex

Abstract

The principles governing the functional organization and development of long-range network interactions in the neocortex remain poorly understood. Using in vivo wide-field and 2-photon calcium imaging of spontaneous activity patterns in mature ferret visual cortex, we find widespread modular correlation patterns that accurately predict the local structure of visually-evoked orientation columns several millimeters away. Longitudinal imaging demonstrates that long-range spontaneous correlations are present early in cortical development prior to the elaboration of horizontal connections, and predict mature network structure. Silencing feed-forward drive through retinal or thalamic blockade does not eliminate early long-range correlated activity, suggesting a cortical origin. Circuit models containing only local, but heterogeneous, connections are sufficient to generate long-range correlated activity by confining activity patterns to a low-dimensional subspace via multi-synaptic short-range interactions. These results suggest that local connections in early cortical circuits can generate structured long-range network correlations that guide the formation of visually-evoked distributed functional networks.

Experience-dependent reorganization drives development of a binocularly unified cortical representation of orientation

“…In the mature visual cortex, neurons that share similar orientation preferences are spatially clustered, defining a modular, but spatially distributed columnar representation of orientation across visual cortex ( Figure 1D, Supplementary Figure 1A To test this possibility, we quantified the spatial clustering by computing the cellular pairwise difference in preferred orientation as a function of distance for stimulation to each eye. Naive animals did not display a higher degree of local scatter in preferred orientation than experienced animals ( Figure 1N, p<0.05 within 100µm unpaired bootstrap test for both Naive and Experienced), consistent with the early columnar organization that has been visualized for spontaneous activity (Smith et al, 2018). Thus, we conclude that hallmarks of the mature visual cortex, such as orientation selectivity, binocular responsiveness, and a columnar architecture, are each already present in visually naive ferrets.…”

“…Orientation-specific microcircuits must already be coarsely established by eyeopening for separate orientation-specific representations to emerge for each eye. In support of this view, chronic imaging in the developing ferret shows that the correlation structure of spontaneous activity patterns before eye-opening predicts the layout of the preferred orientation that becomes evident after eye-opening suggesting that early microcircuits develop without patterned visual experience (Smith et al, 2018). Thus, we conclude that early monocular mismatches reflect the emergence of misaligned monocular network representations, and that early experience is necessary to drive network-scale alignment of these emerging representations.…”

A Model for Navigation in Unknown Environments Based on a Reservoir of Hippocampal Sequences

“…Cortical networks have been described to show stereotyped spontaneous activity patterns on multiple temporal and spatial scales (Raichle et al 2001;Kenet et al 2003). Studies on primary visual cortex have shown that these spontaneous patterns carry over to stimulus processing (Kenet et al 2003;Smith et al 2018) and thus the idea that intrinsic prewiring can be useful for neural information processing is not particularly special for the hippocampus, even more so as sequence like activity can develop in recurrent networks spontaneously (Kitano et al 2002;Aviel et al 2003). It is less obvious, however, whether there is a common computational principle favoring dynamical prestructure.…”

Localized semi-nonnegative matrix factorization (LocaNMF) of widefield calcium imaging data

“…Widefield calcium imaging (WFCI) methods provide a compromise: this approach offers a global view of the (superficial) dorsal cortex, with temporal resolution limited only by the activity indicator, calcium dynamics and camera speeds. Single-cell resolution of superficial neurons is possible using a "crystal skull" preparation [2] but simpler, less invasive thinned-skull preparations that provide spatial resolution of around tens of microns per pixel have become increasingly popular [2][3][4][5][6][7][8][9][10][11][12][13][14]; of course there is also a large relevant literature on widefield voltage and intrinsic signal imaging [15][16][17][18].…”