Organized Toe Maps in Extreme Foot Users

Harriet Dempsey-Jones,Daan B Wesselink,Jason Friedman,Tamar R Makin

doi:10.1016/j.celrep.2019.08.027

Harriet Dempsey-Jones, Daan B Wesselink + Show 2 more

Open Access

https://doi.org/10.1016/j.celrep.2019.08.027

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Abstract

SummaryAlthough the fine-grained features of topographic maps in the somatosensory cortex can be shaped by everyday experience, it is unknown whether behavior can support the expression of somatotopic maps where they do not typically occur. Unlike the fingers, represented in all primates, individuated toe maps have only been found in non-human primates. Using 1-mm resolution fMRI, we identify organized toe maps in two individuals born without either upper limb who use their feet to substitute missing hand function and even support their profession as foot artists. We demonstrate that the ordering and structure of the artists’ toe representation mimics typical hand representation. We further reveal “hand-like” features of activity patterns, not only in the foot area but also similarly in the missing hand area. We suggest humans may have an innate capacity for forming additional topographic maps that can be expressed with appropriate experience.

Highlights

The hand area of the primary somatosensory cortex (SI), and Brodmann area (BA) 3b in particular, contains detailed digit maps, with physically adjacent digits showing greater representational overlap than non-adjacent fingers (Besle et al, 2014; Kaas et al, 1979; Sanchez-Panchuelo et al, 2012; Thakur et al, 2012)
The gross features of the canonical hand representation are highly consistent in humans (Ejaz et al, 2015; Kikkert et al, 2016; Kolasinski et al, 2016), the inter-finger selectivity may be shaped by experience, e.g., digits used more frequently together in daily life show more representational overlap (Ejaz et al, 2015) and vice versa (Gindrat et al, 2015)
We investigated whether extreme habitual foot behavior might associate with organized toe maps in SI, where they have not been found in typically developed humans (Akselrod et al, 2017), they are identified in monkeys (Liao et al, 2016; Nelson et al, 1980)

Summary

Introduction

The hand area of the primary somatosensory cortex (SI), and Brodmann area (BA) 3b in particular, contains detailed digit maps, with physically adjacent digits showing greater representational overlap than non-adjacent fingers (Besle et al, 2014; Kaas et al, 1979; Sanchez-Panchuelo et al, 2012; Thakur et al, 2012) (see Figures 2A and 3C). Displaying exquisite compensatory adaptation, these individuals perform typically manual daily living tasks (e.g., dressing, feeding, and typing) with their feet (see Figures 1A–1C). Both use one foot for dextrous object manipulation and the other for stabilizing. Both are sufficiently skilled with their dextrous foot to allow writing, drawing, and painting to a level that supports their profession as artists (two of only three such foot artists in the UK)

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