Organizing principles of pulvino-cortical functional coupling in humans

Michael J Arcaro,Sabine Kastner,Mark A Pinsk,Janice Chen

doi:10.1038/s41467-018-07725-6

Michael J Arcaro, Sabine Kastner + Show 2 more

Open Access

https://doi.org/10.1038/s41467-018-07725-6

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Abstract

The pulvinar influences communication between cortical areas. We use fMRI to characterize the functional organization of the human pulvinar and its coupling with cortex. The ventral pulvinar is sensitive to spatial position and moment-to-moment transitions in visual statistics, but also differentiates visual categories such as faces and scenes. The dorsal pulvinar is modulated by spatial attention and is sensitive to the temporal structure of visual input. Cortical areas are functionally coupled with discrete pulvinar regions. The spatial organization of this coupling reflects the functional specializations and anatomical distances between cortical areas. The ventral pulvinar is functionally coupled with occipital-temporal cortices. The dorsal pulvinar is functionally coupled with frontal, parietal, and cingulate cortices, including the attention, default mode, and human-specific tool networks. These differences mirror the principles governing cortical organization of dorsal and ventral cortical visual streams. These results provide a functional framework for how the pulvinar facilitates and regulates cortical processing.

Highlights

The primate pulvinar is anatomically and functionally heterogeneous
Though difficult to discern from anatomy alone, such an organization is predicted based on recent physiological studies in monkeys showing that the pulvinar plays a role in synchronizing activity between cortical regions involved in a visual attention task[9]
The organization of cortical coupling within the pulvinar reflected both the distances between cortical areas and their functional specialization. These results demonstrate that the dorsal and ventral pulvinar are major nodes in the often cortically-emphasized dorsal and ventral visual processing streams and illustrate that principles guiding the functional organization of cortex are present within the human pulvinar

Summary

Introduction

The primate pulvinar is anatomically and functionally heterogeneous. Most of our understanding of the pulvinar comes from studies in non-human primates (Supplementary Note 1)[10], and there is only a beginning understanding in the human brain that the pulvinar appears to be similar to other primate species[11,12,13]. This parallels the observation that neighboring cortical areas tend to be interconnected[17,18], and supports the notion that areas that are directly connected are indirectly connected via the thalamus[2,6] Based on such anatomical studies, it might be expected that pulvino-cortical functional interactions reflect cortical distance with neighboring cortical areas interacting with similar parts of the pulvinar. The organization of cortical coupling within the pulvinar reflected both the distances between cortical areas and their functional specialization These results demonstrate that the dorsal and ventral pulvinar are major nodes in the often cortically-emphasized dorsal and ventral visual processing streams and illustrate that principles guiding the functional organization of cortex are present within the human pulvinar. These data highlight the fine-grained organization of pulvinocortical interactions and greatly contribute to our understanding of the human thalamus by illustrating important constraints on the role(s) of the pulvinar in facilitating and regulating cortical processing

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