Corticothalamic Projections Gate Alpha Rhythms in the Pulvinar

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.

The replication principle revisited: a shared functional organization between pulvinar-cortical and cortico-cortical connectivity and its structural and molecular imaging correlates

“…Together, these results reinforce the concept of pulvinar involvement in multimodal sensory integration and top-down attentional processing, consistent with recent literature (Saalmann et al 2012;Benarroch 2015;Fiebelkorn and Kastner 2020;Froesel et al 2021). They also align with the proposed role of pulvinar-cortical connectivity in enhancing communication and synchronization within cortical processing modules in a context-dependent and competitive manner (Rockland et al 1999;Cortes et al 2021Cortes et al , 2024Aussel et al 2023;Bastuji et al 2024).…”

Evolutionary origin of alpha rhythms in vertebrates

“…Interestingly, the frequency of primary rhythms in the visual cortex of mammals correlates with brain size, ranging from 3-6 Hz in mice ( Senzai, et al, 2019 ), 6-12 Hz in cats ( Lörincz et al, 2009 ), to 8-12 Hz in humans. Thus, the emergence of the primate-specific alpha rhythm at 10 Hz might be associated with both the enlargement of the brain and the maturation of circuits in the neocortex and pulvinar ( Cortes, et al, 2021 ).…”

Alpha Oscillations in Resisting Distraction

“…Interestingly, interneurons play a crucial role in generating this phasic activity in the thalamus (see also Hughes et al 2004Hughes et al , 2011Hughes et Crunelli 2005 for additional processes involved in the thalamus). Several studies have also highlighted the involvement of the pulvinar nucleus of the thalamus in regulating cortical alpha rhythms (Cortes et al, 2021;Fiebelkorn et al, 2019;Saalmann et al, 2012Saalmann et al, , 2018. Many in vitro studies have challenged the idea of the thalamus as the sole origin of cortical alpha oscillations.…”