Abstract

Two types of corticothalamic (CT) terminals reach the pulvinar nucleus of the thalamus, and their distribution varies according to the hierarchical level of the cortical area they originate from. While type 2 terminals are more abundant at lower hierarchical levels, terminals from higher cortical areas mostly exhibit type 1 axons. Such terminals also evoke different excitatory postsynaptic potential dynamic profiles, presenting facilitation for type 1 and depression for type 2. As the pulvinar is involved in the oscillatory regulation between intercortical areas, fundamental questions about the role of these different terminal types in the neuronal communication throughout the cortical hierarchy are yielded. Our theoretical results support that the co-action of the two types of terminals produces different oscillatory rhythms in pulvinar neurons. More precisely, terminal types 1 and 2 produce alpha-band oscillations at a specific range of connectivity weights. Such oscillatory activity is generated by an unstable transition of the balanced state network’s properties that it is found between the quiescent state and the stable asynchronous spike response state. While CT projections from areas 17 and 21a are arranged in the model as the empirical proportion of terminal types 1 and 2, the actions of these two cortical connections are antagonistic. As area 17 generates low-band oscillatory activity, cortical area 21a shifts pulvinar responses to stable asynchronous spiking activity and vice versa when area 17 produces an asynchronous state. To further investigate such oscillatory effects through corticothalamo-cortical projections, the transthalamic pathway, we created a cortical feedforward network of two cortical areas, 17 and 21a, with CT connections to a pulvinar-like network with two cortico-recipient compartments. With this model, the transthalamic pathway propagates alpha waves from the pulvinar to area 21a. This oscillatory transfer ceases when reciprocal connections from area 21a reach the pulvinar, closing the CT loop. Taken together, results of our model suggest that the pulvinar shows a bi-stable spiking activity, oscillatory or regular asynchronous spiking, whose responses are gated by the different activation of cortico-pulvinar projections from lower to higher-order areas such as areas 17 and 21a.

Highlights

  • Integrating different visual attributes of an image into a single neuronal representation is a difficult task

  • For this model, cortico-pulvinar projections were divided in striate- and extrastriate-recipient zones to investigate the effect of different signaling pattering of the transthalamic pathway across cortical areas (Figure 2A3)

  • Previous experimental studies have shown that neuronal populations of the pulvinar nucleus possess multiple dynamic activity profiles (Wrobel et al, 2007; Saalmann and Kastner, 2011; Yu et al, 2018; Le et al, 2019)

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Summary

Introduction

Integrating different visual attributes of an image into a single neuronal representation is a difficult task. Throughout evolution, the mammalian visual cortex has solved this computational problem by separating these different features into distinct and parallel processing modules (Bullier, 2001) Interactions between these modules are hierarchical; as more complex levels of organization are created from lower ones (Felleman and Van Essen, 1991; Bullier, 2003; Hegde and Felleman, 2007). Visual processing consists of cortical signals traveling from lower to higher order (HO) areas and vice versa throughout corticocortical connections, whose organization follows a hierarchical pattern This anatomical and functional arrangement of cortical visual areas connected through specific laminar projections is the core of the cortico-centric view of visual integration (Nassi and Callaway, 2009)

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