Evidence for an effector-independent action system from people born without hands

Abstract

Many parts of the visuomotor system guide daily hand actions, like reaching for and grasping objects. Do these regions depend exclusively on the hand as a specific body part whose movement they guide, or are they organized for the reaching task per se, for any body part used as an effector? To address this question, we conducted a neuroimaging study with people born without upper limbs—individuals with dysplasia—who use the feet to act, as they and typically developed controls performed reaching and grasping actions with their dominant effector. Individuals with dysplasia have no prior experience acting with hands, allowing us to control for hand motor imagery when acting with another effector (i.e., foot). Primary sensorimotor cortices showed selectivity for the hand in controls and foot in individuals with dysplasia. Importantly, we found a preference based on action type (reaching/grasping) regardless of the effector used in the association sensorimotor cortex, in the left intraparietal sulcus and dorsal premotor cortex, as well as in the basal ganglia and anterior cerebellum. These areas also showed differential response patterns between action types for both groups. Intermediate areas along a posterior–anterior gradient in the left dorsal premotor cortex gradually transitioned from selectivity based on the body part to selectivity based on the action type. These findings indicate that some visuomotor association areas are organized based on abstract action functions independent of specific sensorimotor parameters, paralleling sensory feature-independence in visual and auditory cortices in people born blind and deaf. Together, they suggest association cortices across action and perception may support specific computations, abstracted from low-level sensorimotor elements.

From Observed Action Identity to Social Affordances

“…Several of the classes therefore have remarkable similarities to the categories described by the intracortical microstimulation studies mentioned previously, and it is plausible to consider them readouts from the neural activity of parieto-frontal cortical regions of freely behaving primates. b A typical effector (e.g., the hand for grasping) can be flexibly replaced by another (e.g., the foot or mouth) in particular circumstances [113].…”

Transforming abstract plans into concrete actions

“…But where in the brain are these abstract representations encoded? In a neuroimaging study, Liu et al (1) address this question by looking at the patterns of brain activation in people born without arms as they reached toward or grasped objects using their toes. The authors then compare these patterns of activation with the activation that emerged in the brains of other individuals who reached toward or grasped those same objects with their hands.…”

“…Liu et al (1) are not the first to look for the neural substrates of abstract representations of the same action performed with different effectors. The study of motor equivalence has a long history in psychology and neuroscience (2)(3)(4)(5)(6), and, since the advent of reliable neuroimaging, investigators have been searching for its neural signature.…”

“…Liu et al (1) are able to rule out these possible alternative explanations, by looking at brain activation associated with reaching and grasping movements made with the toes in people with developmental dysplasia who were born without hands and arms-and comparing the pattern of activation in their brains with that observed in participants with a normal developmental trajectory using their hand to perform the same actions. People who are born without hands and arms often become quite adept at reaching out and grasping objects using their feet.…”

Are reaching and grasping effector-independent? Similarities and differences in reaching and grasping kinematics between the hand and foot

“…For example, during motor planning (Gallivan, McLean, Smith, & Culham, 2011) or execution (Magri, Fabbri, Caramazza, & Lingnau, 2019), brain areas including premotor cortex and superior parietal lobule encode target location whether individuals reached with their hand or made saccades with the eyes toward it (also see Heed, Beurze, Toni, Röder, & Medendorp, 2011;Heed, Leone, Toni, & Medendorp, 2016;Leoné, Heed, Toni, & Pieter Medendorp, 2014). Common activation or activity pattern during reaching and grasping actions is also found between the two hands (Gallivan, McLean, Flanagan, & Culham, 2013;Haar, Dinstein, Shelef, & Donchin, 2017;Turella, Rumiati, & Lingnau, 2020), between the hand and the mouth (Castiello et al, 2000), between the hand and tools (Umiltà et al, 2008;, or between the hand and foot (Heed et al, 2011(Heed et al, , 2016Leoné et al, 2014;Liu, Vannuscorps, Caramazza, & Striem-Amit, 2020). Neurons responding to both hands or hand and eye were also recorded in posterior parietal cortex in non-human primates (Chang, Dickinson, & Snyder., 2008;Diomedi et al, 2020).…”