The spatial extent of anatomical connections within the thalamus varies across the cortical hierarchy in humans and macaques

Abstract

The thalamus is composed of functionally and structurally distinct nuclei. Previous studies have indicated that certain cortical areas may project across multiple thalamic nuclei, potentially allowing them to modulate distributed information flow. However, there is a lack of quantitative investigations into anatomical connectivity patterns within the thalamus. Consequently, it remains unknown if cortical areas exhibit differences in the spread of their thalamic connectivity patterns. To address this knowledge gap, we used diffusion magnetic resonance imaging (dMRI) to compute brain-wide probabilistic tractography using data from 828 healthy adults collected by the Human Connectome Project. To measure the spatial extent of anatomical connectivity patterns within the thalamus, we developed an innovative framework that quantifies the spatial properties of each cortical area’s within-thalamus connectivity patterns. We then leveraged resting-state functional MRI, cortical myelin, and human neural gene expression data to test if the spread of within-thalamus connectivity patterns varied along the cortical hierarchy. These results revealed two broad cortico-thalamic tractography motifs: 1) a sensorimotor cortical motif characterized by focal thalamic connections targeting posterolateral thalamus, which potentially supports fast, feed-forward information flow; and 2) an associative cortical motif characterized by diffuse thalamic connections targeting anteromedial thalamus, which potentially supports slower, feed-back information flow. These results were consistent among human subjects and were also observed in macaques, indicating cross-species generalizability. In summary, these findings demonstrate that sensorimotor and association cortical areas exhibit differences in the spatial extent of their within-thalamus connectivity patterns, which may support functionally-distinct cortico-thalamic information transmission.

A Multimodal Characterization of Low-Dimensional Thalamocortical Structural Connectivity Patterns

“…Additionally, they found that matrix cell regions tend to couple to cortical areas with a lower intrinsic timescale (Müller et al, 2020). Thus, overall both gradients pointed to a differentiation between sensorimotor and transmodal networks, mirroring observations in recent work of a sensorimotor and association ‘motif’ of thalamic cortical patterning (Howell et al, 2023). Extending this work, we illustrated how these motifs may be embedded within the intrinsic organization of the thalamus along two main structurally defined gradients.…”

“…This observation may arise due to the exclusion of the LGN from our thalamic mask (projects to primary visual cortex; Jones, 1985;Leh et al, 2008), and further may be driven by the projections of the Pulvinar encompassing higher-order areas and the visual system (Barron et al, 2015). The distinction of sensorimotor and association areas based on structural and functional connectivity aligned with previous work in humans and animals (Jones, 1998;Mukherjee et al, 2020;Harris et al, 2019;Howell et al, 2023) that illustrated how the thalamus may be a key node in the brain coordinating both sensorimotor and abstract cognitive functions (Shine et al, 2023;Wolff et al, 2021).…”

“…This observation may arise due to the exclusion of the LGN from our thalamic mask (projects to primary visual cortex; Jones, 1985; Leh et al, 2008), and further may be driven by the projections of the Pulvinar encompassing higher-order areas and the visual system (Barron et al, 2015). The distinction of sensorimotor and association areas based on structural and functional connectivity aligned with previous work in humans and animals (Jones, 1998; Mukherjee et al, 2020; Harris et al, 2019; Howell et al, 2023) that illustrated how the thalamus may be a key node in the brain coordinating both sensorimotor and abstract cognitive functions (Shine et al, 2023; Wolff et al, 2021). Moreover, the cortical projection pattern of the principle structural connectivity gradient echoed maps of laminar differentiation and sensory-transmodal axes, patterns possibly linked to cortical maturation during the first two decades of human development (Larsen et al, 2023; Sydnor et al, 2023; Burt et al, 2018b; Margulies et al, 2016).…”