bioRxiv Science⌕ Search

Biology subjects

Contemori, S.

Publications and source records attributed to Contemori, S..

6 recordsLinked to original sources

Subcortical control of reaching in humans

Accurate visually guided reaching requires transformation of target-related photoreceptor responses into precisely coordinated activation of trunk and arm muscles. The cerebral cortex is widely believed to compute the requisite kinematic and musculoskeletal dynamics strategies in humans 1-3, even though vertebrates lacking a cerebral cortex achieve sophisticated visuomotor control 4-6, and brainstem circuits executing coordinated eye and head gaze shifts perform analogous sensorimotor computations in non-human primates 7. Here we used a visuomotor reaching task that yields extremely rapid, "express", target-directed muscle activations 8-10 to test whether a putative subcortical sensorimotor network can compute musculoskeletal dynamics to initiate reaching in humans. We found coordinated express visuomotor responses (EVRs) in task-relevant shoulder, elbow, and bi-articular muscles that reflected both starting posture and target direction in similar patterns to longer latency, presumably cortically mediated, muscle responses. When the task goal was to reach away from the stimulus (i.e. an "anti-reach"; 11) the EVR involved coordinated muscle activation to initiate the hand toward the stimulus location, opposite to the subsequent goal-directed response. The results suggest a unified theory of visuomotor control for reaching and gaze shifts, in which subcortical systems compute musculoskeletal dynamics based on sensory target information and cortically derived context. The results imply that the transformation from motor goals in extrapersonal space into musculoskeletal dynamics can be performed by neural circuitry in humans that does not involve the sensorimotor cortex.

neuroscience↗

Motor decision-making under uncertainty and time pressure

Purposeful movement often requires selection of a particular action from a range of alternatives, but how does the brain represent potential actions so that they can be compared for selection, and how are motor commands generated if movement is initiated before the final goal is identified? According to one hypothesis, the brain averages partially prepared motor plans to generate movement when there is goal uncertainty. This is consistent with the idea that motor decision making unfolds through competition between internal representations of alternative actions. An alternative hypothesis holds that only one movement, which is optimised for task performance, is prepared for execution at any time. Under this conception, decisions about the best motor goal given current information are completed upstream from neural circuits that perform motor planning. To distinguish between these hypotheses, we modified Alhussein and Smith (2021) experiment in which participants had to start reaching toward targets associated with opposite curl force-fields prior to knowing the correct target to reach. Crucially, we forced the participants to initiate movement immediately after target presentation (i.e. mean reaction times [~]250ms) so that they had limited opportunity to deliberate between the available alternatives. We found that the reaching dynamics reflected only those learnt for the selected reach direction, rather than a combination of those for the alternative targets presented, irrespective of the time available to initiate movement. The data are consistent with the conclusion that reaching dynamics were specified downstream of action selection under the target uncertainty conditions of this study. NEW & NOTEWORTHYHere we found no evidence of "motor averaging" of reach dynamics for multiple potential actions when people had to respond as quickly as possible to uncertain target location cues. People exerted forces appropriate for the specific reach direction they selected irrespective of movement initiation time, suggesting that reaching dynamics were specified downstream of action selection.

neuroscience↗

Express visuomotor responses reflect knowledge of both target location and conscious intent during reaches of different amplitudes

When humans reach to visual targets, extremely rapid (~90 ms) bursts of activity can be observed on task-relevant proximal muscles. Such express visuomotor responses are inflexibly locked in time and space to the target and have been proposed to reflect rapid visuomotor transformations conveyed subcortically via the tecto-reticulo-spinal pathway. Previously, we showed that express visuomotor responses are sensitive to explicit cue-driven information about the target, suggesting that the express pathway can be modulated by cortical signals affording contextual pre-stimulus expectations. Here, we show that the express visuomotor system incorporates information about the veridical target-directed reaching metrics and contextual instructions during visuospatial tasks requiring different movement amplitudes. In one experiment, we recorded the activity from two shoulder muscles as participants reached toward targets that appeared at different distances. Longer hand-to-target distances led to larger and more prevalent express visuomotor responses than short-reach targets. This suggests that both the direction and distance of veridical hand-to-target reaches are encoded along the putative subcortical express pathway. In a second experiment, we modulated the movement amplitude by asking the participants to deliberately undershoot, overshoot, or stop (control) at the target. The overshoot and undershoot tasks impaired the generation of large and frequent express visuomotor responses, consistent with the inability of the express pathway to generate responses directed toward non-veridical targets (e.g. anti-reach tasks). Our findings appear to reflect strategic, cortically-driven modulation of the express visuomotor circuit to facilitate rapid and effective response initiation during target-directed actions. SIGNIFICANCE STATEMENTExpress (~90 ms) arm muscle responses that are consistently tuned toward the location of visual stimuli suggest a subcortical contribution to target-directed visuomotor behaviour in humans, potentially via the tecto-reticulo-spinal pathway. This study shows that express muscle responses are modulated appropriately to reach targets at different distances, but generally suppressed when the task required non-veridical responses to overshoot/undershoot the real target. The data suggest that the tecto-reticulo-spinal pathway can be exploited strategically by the cerebral cortex to facilitate rapid initiation of effective responses during a visuospatial task.

neuroscience↗

Cue-driven motor planning facilitates express visuomotor responses in human arm muscles

Humans can produce "express" ([~]100ms) arm muscle responses that are inflexibly locked in time and space to the presentation of a visual target, consistent with subcortical visuomotor transformations via the tecto-reticulo-spinal pathway. These express visuomotor responses are sensitive to explicit cue-driven expectations, but it is unclear at what stage of sensory-to-motor transformation such modulation occurs. Here, we recorded electromyographic activity from shoulder muscles as participants reached toward one of four virtual targets whose physical location was partially predictable from a symbolic cue. In an experiment in which targets could be veridically reached, express responses were inclusive of the biomechanical requirements for reaching the cued locations and not systematically modulated by cue validity. In a second experiment, movements were restricted to the horizontal plane so that the participants could perform only rightward or leftward reaches, irrespective of target position on the vertical axis. Express muscle responses were almost identical for targets that were validly cued in the horizontal direction, regardless of cue validity in the vertical dimension. Together, these findings suggest that the cue-induced enhancements of express responses are dominated by effects at the level of motor plans and not solely via facilitation of early visuospatial target processing. Notably, direct cortico-tectal and cortico-reticular projections exist that are well-placed to modulate pre-stimulus motor preparation state in subcortical circuits. Our results appear to reflect a neural mechanism by which contextually relevant motor plans can be stored within subcortical visuomotor nodes and rapidly released in response to compatible visual inputs. NEW & NOTEWORTHYExpress arm muscle responses to suddenly appearing visual targets for reaching rapid have been attributed to the tecto-reticulo-spinal pathway in humans. We demonstrate that symbolic cues before target presentation can modulate such express arm muscle responses compatibly with the biomechanics of the cued reaching direction and the cue validity. This implies cortically mediated modulation of one or more sensorimotor transformation nodes of the subcortical express pathway.

neuroscience↗

Trial-by-trial modulation of express visuomotor responses induced by symbolic or barely detectable cues

Human cerebral cortex can produce visuomotor responses that are modulated by contextual and task-specific constraints. However, the distributed cortical network for visuomotor transformations limits the minimal response time of that pathway. Notably, humans can generate express visuomotor responses that are inflexibly tuned to the target location and occur 80-120ms from stimulus presentation (stimulus-locked responses, SLRs). This suggests a subcortical pathway for visuomotor transformations involving the superior colliculus and its downstream reticulo-spinal projections. Here we investigated whether cognitive expectations can modulate the SLR. In one experiment, we recorded surface EMG from shoulder muscles as participants reached toward a visual target whose location was unpredictable in control conditions, and partially predictable in cue conditions by extrapolating a symbolic cue (75% validity). Valid symbolic cues led to faster and larger SLRs than control conditions; invalid symbolic cues produced slower and smaller SLRs than control conditions. This is consistent with a cortical top-down modulation of the putative subcortical SLR-network. In a second experiment, we presented high-contrast targets in isolation (control) or ~24ms after low-contrast stimuli, which could appear at the same (valid cue) or opposite (invalid cue) location as the target, and with equal probability (50% cue validity). We observed faster SLRs than control with the valid low-contrast cues, whereas the invalid cues led to the opposite results. These findings may reflect exogenous priming mechanisms of the SLR network, potentially evolving subcortically via the superior colliculus. Overall, our results support both top-down and bottom-up modulations of the putative subcortical SLR network in humans. NEW & NOTEWORTHYExpress visuomotor responses in humans appear to reflect subcortical sensorimotor transformation of visual inputs, potentially conveyed via the tecto-reticulo-spinal pathway. Here we show that the express responses are influenced both by symbolic and barely detectable spatial cues about stimulus location. The symbolic cue-induced effects suggest cortical top-down modulation of the putative subcortical visuomotor network. The effects of barely detectable cues may reflect exogenous priming mechanisms of the tecto-reticulo-spinal pathway.

neuroscience↗

The influence of temporal predictability on express visuomotor responses

Volitional visuomotor responses in humans are generally thought to manifest 100ms or more after stimulus onset. Under appropriate conditions, however, much faster target-directed responses can be produced at upper limb and neck muscles. These "express" responses have been termed stimulus-locked responses (SLRs) and are proposed to be modulated by visuomotor transformations performed subcortically via the superior colliculus. Unfortunately, for those interested in studying SLRs, these responses have proven difficult to detect consistently across individuals. The recent report of an effective paradigm for generating SLRs in 100% of participants appears to change this. The task required the interception of a moving target that emerged from behind a barrier at a time consistent with the target velocity. Here we aimed to reproduce the efficacy of this paradigm for eliciting SLRs and to test the hypothesis that its effectiveness derives from the predictability of target onset time as opposed to target motion per se. In one experiment, we recorded surface EMG from shoulder muscles as participants made reaches to intercept temporally predictable or unpredictable targets. Consistent with our hypothesis, predictably timed targets produced more frequent and stronger SLRs than unpredictably timed targets. In a second experiment, we compared different temporally predictable stimuli and observed that transiently presented targets produced larger and earlier SLRs than sustained moving targets. Our results suggest that target motion is not critical for facilitating the expression of an SLR and that timing predictability does not rely on extrapolation of a physically plausible motion trajectory. These findings provide support for a mechanism whereby an internal timer, probably located in cerebral cortex, primes the processing of both visual input and motor output within the superior colliculus to produce SLRs.

neuroscience↗