Ipsilateral finger representations in the sensorimotor cortex are driven by active movement processes, not passive sensory input

Abstract

Hand and finger movements are mostly controlled through crossed corticospinal projections from the contralateral hemisphere. During unimanual movements, activity in the contralateral hemisphere is increased while the ipsilateral hemisphere is suppressed below resting baseline. Despite this suppression, unimanual movements can be decoded from ipsilateral activity alone. This indicates that ipsilateral activity patterns represent parameters of ongoing movement, but the origin and functional relevance of these representations is unclear. In this study, we asked whether ipsilateral representations are caused by active movement or whether they are driven by sensory input. Participants alternated between performing single finger presses and having fingers passively stimulated while we recorded brain activity using high-field (7T) functional imaging. We contrasted active and passive finger representations in sensorimotor areas of ipsilateral and contralateral hemispheres. Finger representations in the contralateral hemisphere were equally strong under passive and active conditions, highlighting the importance of sensory information in feedback control. In contrast, ipsilateral finger representations in the sensorimotor cortex were stronger during active presses. Furthermore, the spatial distribution of finger representations differed between hemispheres: the contralateral hemisphere showed the strongest finger representations in Brodmann areas 3a and 3b, whereas the ipsilateral hemisphere exhibited stronger representations in premotor and parietal areas. Altogether, our results suggest that finger representations in the two hemispheres have different origins: contralateral representations are driven by both active movement and sensory stimulation, whereas ipsilateral representations are mainly engaged during active movement. NEW & NOTEWORTHY Movements of the human body are mostly controlled by contralateral cortical regions. The function of ipsilateral activity during movements remains elusive. Using high-field neuroimaging, we investigated how human contralateral and ipsilateral hemispheres represent active and passive finger presses. We found that representations in contralateral sensorimotor cortex are equally strong during both conditions. Ipsilateral representations were mostly present during active movement, suggesting that sensorimotor areas do not receive direct sensory input from the ipsilateral hand.

Similar somatotopy for active and passive digit representation in primary somatosensory cortex

“…While these tasks afford different forms of sensory feedback, hand position, motor signals, task demands, and attentional requirements, we hypothesised that resulting digit somatotopy would be similar, because despite differing types or amount of input, all inputs feed into somatotopically restricted regions (Kuehn et al, 2017;Qi & Kaas, 2004 ; also see Discussion). However, consistent with Berlot et al, (2019), increased somatosensory input in the active condition was predicted to lead to greater overall activity in the active task, compared to the passive.…”

“…As clearly demonstrated in Supplementary Figure 3, activity levels were greater in the active task in comparison to the passive task, as confirmed in a paired t-test (averaged activity across all ROIs in the two tasks; t(14)=2.85, p=0.013). This result could be confounded by the fact that the travelling-wave paradigm was more similar to the active task (involved active movement using the same button box), although increased activity has also been reported in previous studies (Berlot et al, 2019;Wiestler et al, 2011).…”

“…As an example, in a single digit tapping task, movement of digit four will activate skin stretch and deep proprioceptors in the palm, as well as causing some degree of enslaved movements in digits three and five (and the resulting sensory inputs from these movements). Aligning with this idea, active tasks have been previously demonstrated to produce greater overall SI activation compared to passive stimulation (Berlot, Prichard, Reilly, Ejaz, & Diedrichsen, 2019;Wiestler, Mcgonigle, & Diedrichsen, 2011). Whilst these concerns are valid, it may also be the case that these biomechanical constraints influence the basic SI organisation, and that through incorporating active tasks to study SI processing we can shed light on these organisational principles (as elaborated in the Discussion below).…”

“…During the active task, participants were required to move individual digits by making button presses on a MRI-safe keyboard with five keys (Berlot et al, 2019). The digit to be moved in the upcoming block was indicated by a visual display of five grey bars, with one highlighted green -indicating the digit to be moved during the upcoming block (see figure 1 left).…”

“…Flor et al, 1995;Makin, Scholz, Henderson Slater, Johansen-Berg, & Tracey, 2015). For instance, multivariate measures reveal similar hand representational structure across SI and MI (Berlot et al, 2019), though SI but not M1 is known to have highlyordered digit somatotopy (Huber et al, 2018).…”