Somatosensory cortex of macaque monkeys is designed for opposable thumb

Lazar, Leslee; Chand, Prem; Rajan, Radhika; Mohammed, Hisham; Jain, Neeraj

doi:10.1093/cercor/bhac061

“…Most neurons in the BA 3b thumb representation specifically respond to tactile stimulation of the thumb but not to tactile stimulation of other fingers and interconnect only sparsely to other digit representations. Also in macaque monkeys, the thumb representation may act as an independent module processing selective information, whereas information content is more distributed between other fingers ( Lazar et al, 2022 ). This may be linked to its special role for tool use.…”

Section: Discussionmentioning

confidence: 99%

The 3D Structural Architecture of the Human Hand Area Is Nontopographic

Doehler

¹

,

Northall

²

,

Liu

³

et al. 2023

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The functional topography of the human primary somatosensory cortex (S1) hand area is a widely studied model system to understand sensory organization and plasticity. It is so far unclear whether or not the underlying 3D structural architecture also shows a topographic organization. We used 7T MRI data to quantify layer-specific myelin, iron and mineralization in relation to population receptive field maps of individual finger representations in Brodman area 3b (BA 3b) of human S1 in female and male younger adults. This 3D description allowed us to identify a characteristic profile of layer-specific myelin and iron deposition in the BA 3b hand area, but revealed an absence of structural differences, an absence of low-myelin borders, and high similarity of 3D microstructure profiles between individual fingers. However, structural differences and borders were detected between the hand and face areas. We conclude that the 3D structural architecture of the human hand area is non-topographic, unlike in some monkey species, which suggests a high degree of flexibility for functional finger organization and a new perspective on human topographic plasticity.SIGNIFICANCE STATEMENT:Using ultra-high field MRI, we provide the first comprehensivein vivodescription of the 3D structural architecture of the human BA 3b hand area in relation to functional population receptive field (pRF) maps. High similarity of precise finger-specific 3D profiles, together with an absence of structural differences and an absence of low-myelin borders between individual fingers, reveal the 3D structural architecture of the human hand area to be non-topographic. This suggests reduced structural limitations to cortical plasticity and reorganization, and allows for shared representational features across fingers.

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“…Most neurons in the BA 3b thumb representation specifically respond to tactile stimulation of the thumb, but not to tactile stimulation of other fingers, and interconnect only sparsely to other digit representations. Also in macaque monkeys, the thumb representation may act as an independent module processing selective information, whereas information content is more distributed between other fingers (Lazar et al, 2023). This may be linked to its special role for tool use.…”

Section: Discussionmentioning

confidence: 99%

“…Also in macaque monkeys, the thumb representation may act as an independent module processing selective information, whereas information content is more distributed between other fingers (Lazar et al, 2023). This may be linked to its special role for tool use.…”

Section: Topographic 3d Structural Architecture Of Ba 3b Hand and Fac...mentioning

confidence: 99%

The 3D Structural Architecture of the Human Hand Area is Non-Topographic

Doehler

¹

,

Northall

²

,

Liu

³

et al. 2022

Preprint

View full text Add to dashboard Cite

The functional topography of the human primary somatosensory cortex (S1) hand area is a widely studied model system to understand sensory organization and plasticity. It is so far unclear whether or not the underlying 3D structural architecture also shows a topographic organization. We used 7T MRI data to quantify layer-specific myelin, iron and mineralization in relation to population receptive field maps of individual finger representations. This 3D description allowed us to identify a characteristic profile of layer-specific myelin and iron deposition in the S1 hand area, but revealed an absence of structural differences between individual finger representations, and an absence of low-myelin borders between individual fingers. Both, however, were detected between the hand and the face areas. Using markers of responsivity, precision and sensorimotor integration, we additionally phenotyped these microstructural features with respect to their relation to BOLD signal change and behavior. We conclude that the 3D structural architecture of the human hand area is non-topographic, other than in some monkey species, which suggests a high degree of flexibility for functional finger organization and plasticity in humans.

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“…A possible explanation for this finding comes from a recent study that observed within area 3b of S1 a homogeneous 3D structural architecture between digits 2-5, excluding the thumb (Doehler et al, 2023). Greater independence of the thumb has also been observed within area 3b of macaque monkeys (Lazar et al, 2023). It is unlikely that this independence holds for area 1, where integration across fingers is known to occur.…”

Section: Rubber Hand Illusion Strength Is Associated With Attenuated ...mentioning

confidence: 96%

Functional displacement of cortical neuromagnetic somatosensory responses: enhancing embodiment in the rubber hand illusion

Isabella,

D’Alonzo,

Mioli

et al. 2023

Preprint

0

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The integration of an artificial limb as part of one’s body involves complex neuroplastic changes resulting from various sensory inputs to the brain. While sensory feedback is known to be crucial for embodiment, current evidence points merely to the attenuation of somatosensory processing, while the positive contributions of somatosensory areas to embodiment remain unknown. This study investigated the relationship between embodiment and adaptive neuroplasticity of early-latency somatosensory evoked fields (SEFs) in the primary somatosensory cortex (S1) following the Rubber Hand Illusion (RHI), known to induce short-term artificial limb embodiment. Nineteen healthy adults underwent neuromagnetic recordings during electrical stimulation of the little finger and thumb, before and after the RHI. We found a displacement of early SEF sources. In particular, we observed a correlation between the extent of rubber hand embodiment and specific changes to the m20 component (magnetic equivalent to the N20) in Brodmann Area 3b: a larger displacement and a greater reduction in m20 magnitude predicted the amount of embodiment, highlighting an important functional contribution of this first cortical input. Furthermore, we observed a posteriorly directed m35 displacement towards Area 1, known to be important for visual integration during touch perception (Rosenthal et al., 2023). Our finding that the larger displacement for the m35 did not correlate with the extent of embodiment implies a functional distinction between neuroplastic changes across these two components and areas in their contributions to successful artificial limb embodiment: (i) the earlier neuroplastic changes to m20 may shape the extent of artificial limb ownership, and (ii) the posteriorward shift of the m35 into Area 1 is suggestive of a mechanistic contribution to early visual-tactile integration that initially establishes the embodiment. Taken together, these findings suggest that multiple distinct changes occur during early-latency SEFs and their displacement in S1 last beyond the duration of the illusion and are important for the successful integration of an artificial limb within the body representation.

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Somatosensory cortex of macaque monkeys is designed for opposable thumb

Cited by 4 publications

References 57 publications

The 3D Structural Architecture of the Human Hand Area Is Nontopographic

The 3D Structural Architecture of the Human Hand Area Is Nontopographic

The 3D Structural Architecture of the Human Hand Area is Non-Topographic

Functional displacement of cortical neuromagnetic somatosensory responses: enhancing embodiment in the rubber hand illusion

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