Self-organization of modular activity in immature cortical networks

Mulholland, Haleigh N.; Kaschube, Matthias; Smith, Gordon B.

doi:10.1038/s41467-024-48341-x

Cited by 4 publications

(1 citation statement)

References 87 publications

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“…Computational and experimental results have suggested that prior to the developmental emergence of long- range horizontal axons (Durack and Katz 1996), such long-range correlated networks can arise through purely local interactions. Models in the form of local excitation / lateral inhibition (LELI) can account for both the presence of modular functional activity as well as millimeter-scale correlations (Smith et al 2018), and are consistent with the ability of the early cortex to self-organize unstructured inputs (Mulholland, Kaschube, and Smith 2024).…”

Section: Introductionmentioning

confidence: 79%

Stereotyped spatiotemporal dynamics of spontaneous activity in visual cortex prior to eye-opening

Kettlewell,

Sederberg,

Smith

2024

Preprint

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Over the course of development, functional sensory representations emerge in the visual cortex. Prior to eye-opening, modular patterns of spontaneous activity form long-range networks that may serve as a precursor for mature network organization. Although the spatial structure of these networks has been well studied, their temporal features, which may contribute to their continued plasticity and development, remain largely uncharacterized. To address this, we imaged hours of spontaneous network activity in the visual cortex of developing ferrets of both sexes utilizing a fast calcium indicator (GCaMP8m) and widefield imaging at high temporal resolution (50Hz), then segmented out spatiotemporal events. The spatial structure of this activity was highly modular, exhibiting spatially segregated active domains consistent with prior work. We found that the vast majority of events showed a clear dynamic component in which modules activated sequentially across the field of view, but only a minority of events were well-fit with a linear traveling wave. We found that spatiotemporal events occur in repeated and stereotyped motifs, reoccurring across hours of imaging. Finally, we found that the most frequently occurring single-frame spatial activity patterns were predictive of future activity patterns over hundreds of milliseconds. Together, our results demonstrate that spontaneous activity in the early developing cortex exhibits a rich spatiotemporal structure, suggesting a potential role in the maturation and refinement of future functional representations.Significance statementUnderstanding the temporal dynamics underlying the network structure in early development is critical for understanding network function and plasticity. By imaging hours of spontaneous cortical activity, we show strong evidence that the vast majority of spontaneous neural activity is dynamic with repeated and complex spatiotemporal patterns with stereotyped structure across hours. This suggests the potential for Hebbian learning in the development and refinement of functional visual representations. We also find that frequently occurring spatial activity patterns are predictive of subsequent activity for up to one second, which may indicate attractor dynamics in spontaneous activity. Our findings characterize key features of the temporal structure of spontaneous activity in visual cortex early in development and deepen our understanding of developing neural networks.

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Section: Introductionmentioning

confidence: 79%

Stereotyped spatiotemporal dynamics of spontaneous activity in visual cortex prior to eye-opening

Kettlewell,

Sederberg,

Smith

2024

Preprint

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Coherent cortical representations develop after experience via feedforward-recurrent circuit alignment

Lempel

Fitzpatrick

2023

Preprint

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Selective and reliable cortical sensory representations depend on synaptic interactions between feedforward inputs, conveying information from lower levels of the sensory pathway, and recurrent networks that reciprocally connect neurons functioning at the same hierarchical level. Here we explore the development of feedforward/recurrent interactions in primary visual cortex of the ferret that is responsible for the representation of orientation, focusing on the feedforward inputs from cortical layer 4 and its relation to the modular recurrent network in layer 2/3 before and after the onset of visual experience. Using simultaneous laminar electrophysiology and calcium imaging we found that in experienced animals, individual layer 4 and layer 2/3 neurons exhibit strongly correlated responses with the modular recurrent network structure in layer 2/3. Prior to experience, layer 2/3 neurons exhibit comparable modular correlation structure, but this correlation structure is missing for individual layer 4 neurons. Further analysis of the receptive field properties of layer 4 neurons in naive animals revealed that they exhibit very poor orientation tuning compared to layer 2/3 neurons at this age, and this is accompanied by the lack of spatial segregation of ON and OFF subfields, the definitive property of layer 4 simple cells in experienced animals. Analysis of the response dynamics of layer 2/3 neurons with whole-cell patch recordings confirms that individual layer 2/3 neurons in naive animals receive poorly-selective feedforward input that does not align with the orientation preference of the layer 2/3 responses. Further analysis reveals that the misaligned feedforward input is the underlying cause of reduced selectivity and increased response variability that is evident in the layer 2/3 responses of naive animals. Altogether, our experiments indicate that the onset of visual experience is accompanied by a critical refinement in the responses of layer 4 neurons and the alignment of feedforward and recurrent networks that increases the selectivity and reliability of the representation of orientation in V1.

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Iso-orientation bias of layer 2/3 connections: the unifying mechanism of spontaneous, visually and optogenetically driven V1 dynamics

Rózsa,

Cagnol,

Antolík

2024

Preprint

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Functionally specific long-range lateral connectivity in layer 2/3 of the primary visual cortex (V1) supports the integration of visual information across visual space and shapes spontaneous, visual and optogenetically driven V1 activity. However, a comprehensive understanding of how these diverse cortical regimes emerge from this underlying cortical circuitry remains elusive. Here we address this gap by showing how the same model assuming moderately iso-orientation biassed long-range cortical connectivity architecture explains diverse phenomena, including (i) range of visually driven phenomena, (ii) modular spontaneous activity, (iii) the propagation of spontaneous cortical waves, and (iv) neural responses to patterned optogenetic stimulation. The model offers testable predictions, including presence of slower and iso-tropic spontaneous wave propagation in layer 4 and non-monotonicity of optogenetically driven cortical response to increasingly larger disk of illumination. We thus offer a holistic framework for studying how cortical circuitry governs information integration across multiple operating regimes.

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Self-organization of modular activity in immature cortical networks

Cited by 4 publications

References 87 publications

Stereotyped spatiotemporal dynamics of spontaneous activity in visual cortex prior to eye-opening

Stereotyped spatiotemporal dynamics of spontaneous activity in visual cortex prior to eye-opening

Coherent cortical representations develop after experience via feedforward-recurrent circuit alignment

Iso-orientation bias of layer 2/3 connections: the unifying mechanism of spontaneous, visually and optogenetically driven V1 dynamics

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