Biology subjects

Carroll, T. J.

Publications and source records attributed to Carroll, T. J..

36 records · Page 2Linked to original sources

bioRxiv2023

Dopamine increases accuracy and lengthens deliberation time in explicit motor skill learning.

Although animal research implicates a central role for dopamine in motor skill learning, a direct causal link has yet to be established in neurotypical humans. Here, we tested if a pharmacological manipulation of dopamine alters motor learning, using a paradigm which engaged explicit, goal-directed strategies. Participants (27 females, 11 males, aged 18-29 years) first consumed either 100mg of Levodopa (n=19), a dopamine precursor that increases dopamine availability, or placebo (n=19). Then, during training, participants learnt the explicit strategy of aiming away from presented targets by instructed angles of varying sizes. Targets shifted mid-movement by the instructed aiming angle. Task success was thus contingent upon aiming accuracy. The effect of the dopamine manipulations on skill learning was assessed during training, and at an overnight follow-up. Increasing dopamine availability improved aiming accuracy and lengthened reaction times, particularly for larger, more difficult aiming angles, both at training, and at follow-up. Results support the proposal that dopamine is important in decisions to engage instrumental motivation to optimise performance, particularly when learning to execute goal-directed strategies in motor skill learning.

neuroscience↗

bioRxiv2022

A complex reach direction rule that delays reaction time causes alternating excitation and inhibition in express muscle responses and corticospinal excitability

The dynamics of muscle activation during fast visually guided reaching are suggestive of two neural control signals; an early signal that acts at "express" latencies in response to the visual stimulus, and a longer latency signal that executes a strategic reach plan. Here we developed a task designed to temporally isolate the express visuomotor response from the longer latency muscle response, and to characterize the time course of corticospinal excitability changes in the express response time window when the late voluntary response is delayed. We tested this by measuring electromyograms (EMG) and changes in Motor Evoked Potential (MEP) amplitudes following Transcranial Magnetic Stimulation (TMS) of the motor cortex, as participants reached either towards or away from visual targets. Crucially, the information about the task rule was provided by the luminance of the target itself, and so was unknown to the subject until the instant of target presentation. This feature delayed reaction times, likely because additional (presumably cortical) processing was required to interpret and apply the rule before formation of a goal directed reach plan. The earliest EMG responses to target presentation occurred with a 70-105 ms time window, and were oriented to bring the hand toward the location of the target. However, there was also a slightly later response that was also time-locked to target appearance in a 105-140 ms time window. This second response was "reciprocal" to the first, such that it was oriented to take the hand in the direction opposite from the target. In some participants, additional oscillating cycles were apparent after the first two target-related responses. These multiphasic express visuomotor responses were nearly identical in both pro- and anti-reach conditions. These muscle activity responses were generally reflected in the temporal pattern of corticospinal excitability modulations in experiment two. Indeed, the MEP and background EMG responses showed an alternating pattern similar to that in experiment one, although the effect was clearer in the anti-reach than the pro-reach condition. Overall, the data show that the express and voluntary responses are indeed distinct neural control signals, which supports the hypothesis that at least two separate neural pathways (one slow and one fast) contribute to the control of visually guided reaching. The properties of the fast pathway are consistent with a tecto-reticulospinal pathway, while those of the slow pathway are consistent with a transcortical loop.

neuroscience↗

bioRxiv2022

A subcortical origin for rapid, target-oriented corticospinal excitability changes during visually guided reaching

During visually guided reaching, proximal limb muscles can be activated within 80 ms of target appearance. Such "express" visuomotor responses are temporally aligned with target appearance rather than movement onset, and invariably tuned towards the direction of the visual target regardless of the instructed reach direction. These features prompt the hypothesis that express visuomotor responses are driven by a subcortical pathway. We tested this by measuring the changes in Motor Evoked Potential (MEP) size following Transcranial Magnetic Stimulation (TMS) or Transcranial Electrical Stimulation (TES) of the motor cortex, as participants reached either towards or away from visual targets. We found that 70-80 ms after target presentation, MEPs in a primary shoulder flexor muscle (pectoralis major) were oriented towards the target direction regardless of whether the participant subsequently reached towards or away from the target. Similar target-oriented MEP modulations occurred in posterior deltoid and biceps brachii muscles, whereas MEPs in a finger muscle were affected neither by target nor reach direction. Critically, there were no significant differences in modulation of responses to TMS versus TES across all reaching conditions, which suggests that the target-oriented modulation occurs downstream of the motor cortex output neurons. Combined, our results are consistent with a subcortical rather than cortical origin for the earliest changes in corticospinal excitability following visual target onset. A prime candidate for such subcortical modulation includes the superior colliculus and reticular formation.

neuroscience↗

bioRxiv2022

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↗

bioRxiv2022

The effects of crank power and cadence on muscle fascicle shortening velocities, muscle activations and joint-powers during cycling.

Whilst people typically chose to locomote in most economical fashion, during cycling on a bicycle they will, unusually, chose cadences that are higher than metabolically optimal. Empirical measurements of the intrinsic contractile properties of the vastus lateralis (VL) muscle during submaximal cycling suggest that the cadences that people prefer (i.e., self-selected cadences: SSC) allow for optimal muscle fascicle shortening velocity for the production of knee extensor muscle power. It remains unclear, however, whether this is consistent across different power outputs where SSC is known to might be affected. We examined the effect of cadence and external power requirements on muscle neuromechanics and joint powers during cycling. VL fascicle shortening velocities, muscle activations and joint-specific powers were measured during cycling between 60 and 120rpm (and the SSC), while participants produced 10%, 30%, and 50% of peak maximal power. VL shortening velocity increased as cadence increased but was similar across the different power outputs. Although no differences were found in the distribution of joint powers across cadence conditions, the absolute knee joint power increased with increasing crank power output. Muscle fascicle shortening velocities increase in VL at the SSC as pedal power demands increase from submaximal to maximal cycling. It therefore seems highly unlikely that preferred cadence is primarily driven by the desire to maintain "optimal" muscle fascicle shortening velocities. A secondary analysis of muscle activation patterns revealed that minimizing muscle activation is likely more important when choosing a cadence for given pedal power demand.

physiology↗

bioRxiv2022

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↗

bioRxiv2021

Engagement of the contralateral limb can enhance the facilitation of motor output by loud acoustic stimuli

When intense sound is presented during light muscle contraction, inhibition of the corticospinal tract is observed. During action preparation, this effect is reversed, with sound resulting in excitation of the corticospinal tract. We investigated how the combined maintenance of a muscle contraction during preparation for a ballistic action impacts the magnitude of the facilitation of motor output by a loud acoustic stimulus (LAS) - a phenomenon known as the StartReact effect. Participants executed ballistic wrist flexion movements and a LAS was presented simultaneously with the imperative signal in a subset of trials. We examined whether the force level or muscle used to maintain a contraction during preparation for the ballistic response impacted reaction time and/or the force of movements triggered by the LAS. These contractions were sustained either ipsilaterally or contralaterally to the ballistic response. The magnitude of facilitation by the LAS was greatest when low force flexion contractions were maintained in the limb contralateral to the ballistic response during preparation. There was little change in facilitation when contractions recruited the contralateral extensor muscle, or when they were sustained in the same limb that executed the ballistic response. We conclude that a larger network of neurons which may be engaged by a contralateral sustained contraction prior to initiation may be recruited by the LAS, further contributing to the motor output of the response. These findings may be particularly applicable in stroke rehabilitation where engagement of the contralesional side may increase the benefits of a LAS to the functional recovery of movement.

neuroscience↗

bioRxiv2021

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↗

bioRxiv2020

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↗

bioRxiv2020

Proliferation control of kidney interstitial cells

Expansion of interstitial cells in the adult kidney is a hallmark of chronic disease, whereas their proliferation during fetal development is necessary for organ formation. An intriguing difference between adult and neonatal kidneys is that the neonatal kidney has the capacity to control interstitial cell proliferation when the target number has been reached. In this study, we define the consequences of inactivating the TGF{beta}/Smad response in the interstitial cell lineage. We find that pathway inactivation through loss of Smad4 leads to over-proliferation of interstitial cells regionally in the kidney medulla. Genetic and molecular interaction studies showed that Smad3/4 participates in the Wnt/{beta}-catenin signaling pathway, which is responsible for promoting proliferation of interstitial cells. Specifically, Smad4 is required for the expression of the Wnt feedback inhibitor Apcdd1, and based on these findings we propose a model for interstitial cell proliferation control in which the Wnt/{beta}-catenin proliferative signal is attenuated by TGF{beta}/Smad signaling to ensure that proliferation ceases when the target number of interstitial cells has been reached in the neonatal medulla. Summary statementThis study describes a novel function for TGF{beta} signaling in the developing renal interstitium. Mice with Foxd1-Cre-mediated deletion of Smad4 have interstitial expansion and activated Wnt signaling.

developmental biology↗

bioRxiv2020

Characterization of interstitial heterogeneity in the developing kidney

Kidney formation requires the coordinated growth of multiple cell types including the collecting ducts, nephrons, vasculature and interstitium. There has been a long-held belief that interactions between the progenitors of the collecting ducts and nephrons are primarily responsible for development of this organ. However, over the last several years, it has become increasingly clear that multiple aspects of kidney development require signaling from the interstitium. How the interstitium orchestrates these various roles is still poorly understood. We show that during development, the interstitium is a highly heterogeneous, patterned population of cells that occupies distinct positions correlated to the adjacent parenchyma. Our analysis indicates that the heterogeneity is not a mere reflection of different stages in a linear developmental trajectory but instead represents several novel differentiated cell states. Further, we find that beta-catenin has a cell autonomous role in the development of a medullary subset of the interstitium and that this non-autonomously affects the development of the adjacent epithelia. These findings suggest the intriguing possibility that the different interstitial subtypes may create microenvironments that play unique roles in development of the adjacent epithelia and endothelia. Graphical AbstractThe developing interstitium is a highly heterogeneous, patterned population of cells that occupies distinct positions correlated to the adjacent parenchyma. O_FIG O_LINKSMALLFIG WIDTH=161 HEIGHT=200 SRC="FIGDIR/small/973966v1_ufig1.gif" ALT="Figure 1"> View larger version (57K): org.highwire.dtl.DTLVardef@1c79dc3org.highwire.dtl.DTLVardef@469934org.highwire.dtl.DTLVardef@f43787org.highwire.dtl.DTLVardef@1698bd6_HPS_FORMAT_FIGEXP M_FIG C_FIG

developmental biology↗

bioRxiv2019

Asynchronous mixing of kidney progenitor cells potentiates nephrogenesis in organoids

Recent years have seen rapid advances in directed differentiation of human pluripotent stem cells (PSCs) to kidney cells. However, a fundamental difficulty in emulating kidney tissue formation is that kidney development is iterative. Recent studies argue that the human nephron forms through gradual contribution of nephron progenitor cells whose differentiation fates depend on the time at which they are recruited. We show that the majority of PSC-derived nephron progenitor cells differentiated in a short wave in organoid formation and to improve fidelity of PSC-derived organoids, we emulated the asynchronous mix found in the fetal kidney by combining cells differentiated at different times in the same organoid. Asynchronous mixing promoted nephrogenesis, and lineage marking data showed that proximal and distal nephron components preferentially derive from cell populations differentiated at distinct times. When engrafted under the kidney capsule these heterochronic organoids were vascularized and displayed essential features of kidney tissue. Micro-CT and injection of a circulating vascular marker demonstrated that engrafted kidney tissue was connected to the systemic circulation by 2 weeks after engraftment. Proximal tubule glucose uptake was confirmed using intravenous injection of fluorescent dextran. Despite these promising measures of graft function, overgrowth of stromal cells prevented long-term study, and we propose that this is a technical feature of the engraftment procedure rather than a specific shortcoming of the directed differentiation because kidney organoids derived from primary cells and whole embryonic kidneys develop the same stromal overgrowth when engrafted under the kidney capsule.

developmental biology↗

bioRxiv2019

Rapid recalibration of temporal order judgements: Response bias accounts for contradictory results

Recent findings indicate that timing perception is systematically changed after only a single presentation of temporal asynchrony. This effect is known as rapid recalibration. In the synchrony judgement task, similar timing relationships in consecutive trials seem more synchronous (positive rapid recalibration; Van der Burg et al., 2013, 2015). Interestingly, the direction of this effect is reversed for temporal order judgements (negative rapid recalibration; Roseboom, 2019). We aimed to determine whether negative rapid recalibration of temporal order judgements (TOJs) reflects genuine rapid temporal recalibration, or a choice-repetition bias unrelated to timing perception. In our first experiment we found no evidence of rapid recalibration of TOJs, but positive rapid recalibration of associated confidence. This suggests that timing perception had rapidly recalibrated, but that this was undetectable in TOJs, plausibly because the positive recalibration effect was obfuscated by a large negative bias effect. In our second experiment, we dissociated participants previous TOJ from the most recently presented timing relationship, mitigating the choice-repetition bias effect, and found evidence of positive rapid recalibration of TOJs. We therefore conclude that timing perception is rapidly recalibrated positively for both synchrony and temporal order judgements. It remains unclear whether rapid recalibration occurs at the level of sensory processing, leading to similar effects in all subsequent judgements, or reflects a generalised decision-making strategy.

neuroscience↗

bioRxiv2019

Task errors drive memories that improve sensorimotor adaptation.

Traditional views on how humans adapt movements to perturbations of sensory feedback emphasize a fundamental role for automatic, implicit correction of sensory prediction errors. However, it is now clear that adaptive behaviour also involves deliberate, strategic movement corrections. Such strategic processes have recently been argued to underlie the latent retention of sensorimotor adaptation, evident in improved adaptation to previously encountered perturbations; a phenomenon termed "savings". It remains unclear, however, whether savings results from prior experience of sensory prediction errors, task errors, or both. Here, we used perturbations of target locations and hand position feedback during reaching to dissociate the contributions of task and sensory prediction errors to latent sensorimotor memory. We show that prior learning to correct for task errors is required to improve adaptation to rotated hand position feedback, whereas a history of sensory prediction errors is neither sufficient nor obligatory for savings. A history of correcting for task errors, induced by experimentally perturbing the target location instead of perturbing sensory feedback of movement, improved adaptation to visuomotor perturbations that were never before encountered. Limiting movement preparation time further showed that this learning consists of two distinct components: 1) a strategic component that is flexible enough to facilitate corrective responses in the opposite direction, but that requires substantial preparation time, and 2) a set of inflexible, cached, stimulus-response associations between targets and reach directions, that can be expressed under time-pressure when similar task conditions are experienced. The results emphasise that adaptive responses to sensorimotor perturbations take multiple forms.

neuroscience↗

bioRxiv2018

Molecular determinants of WNT9b responsiveness in nephron progenitor cells

Primed nephron progenitor cells (NPCs) appear in metanephric mesenchyme by Ell.5 and differentiate in response to the inductive WNT9b signal from the ureteric bud. However, the NPC WNT-receptor complex is unknown. We obtained M15 cells from E10.5 mesonephric mesenchyme and systematically analyzed components required for canonical WNT9b-responsiveness. When M15 cells were transfected with a ({beta}-catenin luciferase reporter plasmid, exposure to recombinant WNT9b resulted in minimal luciferase activity. We then analyzed mRNA-expression of WNT-pathway components and identified Fzdl-6 and Lrp6 transcripts but not RSPO1. When M15 cells were treated with recombinant RSPO1 the response to transfected WNT9b was augmented 4.8-fold. Co-transfection of M15 cells with Fzd5 (but no other Fzd family member) further increased the WNT9b signal to 16.8-fold and siRNA knockdown of Fzd5 reduced the signal by 52%. Knockdown of Lrp6 resulted in 60% WNT9b signal reduction. We confirmed Fzd5, Lrp6 and RSPO1 rrtRNA expression in CITED1(+) NPCs from E15.5 embryonic mouse kidney. Thus, while many WNT signaling-pathway components are present by E10.5, optimum responsiveness of Ell.5 cap mesenchyme requires that NPCs acquire RSPO1, FZD5 and LRP6.\n\nSummary StatementResponsiveness to the inductive WMT9b signal from ureteric bud is crucial for nephrogenesis. Here we analyze the molecules needed to prime nephron progenitor cells in embryonic mouse kidney.

developmental biology↗

bioRxiv2018

Unilateral movement preparation causes task-specific modulation of TMS responses in the passive, opposite limb.

Corticospinal excitability is modulated for muscles on both sides of the body during unilateral movement preparation. For the effector, there is a progressive increase in excitability, and a shift in direction of muscle twitches evoked by transcranial magnetic stimulation (TMS) toward the impending movement. By contrast, the directional characteristics of excitability changes in the opposite (passive) limb have not been fully characterized. Here we assessed how preparation of voluntary forces towards four spatially distinct visual targets with the left wrist alters muscle twitches and motor evoked potentials (MEPs) elicited by TMS of left motor cortex. MEPs were facilitated significantly more in muscles homologous to agonist rather than antagonist muscles in the active limb, from 120 ms prior to voluntary EMG onset. Thus, unilateral motor preparation has a directionally-specific influence on pathways projecting to the opposite limb that corresponds to the active muscles rather than the direction of movement in space. The directions of TMS-evoked twitches also deviated toward the impending force direction of the active limb, according to muscle-based coordinates, following the onset of voluntary EMG. The data indicate that preparation of a unilateral movement increases task-dependent excitability in ipsilateral motor cortex, or its downstream projections, that reflect the forces applied by the active limb in an intrinsic (body-centered), rather than an extrinsic (world-centered), coordinate system. The results suggest that ipsilateral motor cortical activity prior to unilateral action reflects the state of the active limb, rather than subliminal motor planning for the passive limb.

neuroscience↗

bioRxiv2016

The primary motor cortex is critical for the retention of implicit sensorimotor adaptation

Sensorimotor adaptation, or adaptation of movements to external perturbations, is thought to involve the primary motor cortex (M1). In addition to implicit error-driven remapping, explicit re-aiming strategies also contribute to sensorimotor adaptation. However, no studies to date have examined the role of M1 in implicit learning in isolation from explicit strategies. Because the application of explicit strategies requires time, it is possible to emphasise implicit learning by controlling the time available to prepare movement. Here, we examined the role of M1s role in implicit adaptation to rotated visual feedback whilst suppressing the use of explicit re-aiming strategies by limiting movement preparation times to less than 350ms. Perturbing M1 activity via single-pulse TMS during adaptation to a 30 {degrees} rotation of visual feedback did not alter the rate or extent of error compensation, but elicited poorer retention in post-adaptation trials with no perturbation. This work shows that M1 is critical in the retention of new visuomotor maps as a result of implicit adaptation to a perturbation in sensory feedback when strategic error correction processes are suppressed.\n\nHighlightsO_LIAdaptation of movements to perturbations occurs through explicit and implicit processes.\nC_LIO_LIHere, explicit strategies were suppressed by shortening movement preparation time.\nC_LIO_LIPerturbing motor cortex (M1) with TMS selectively impaired retention but not acquisition of sensorimotor adaptation.\nC_LIO_LIM1 plays a crucial role in retention of sensorimotor adaptation obtained via implicit learning.\nC_LI

neuroscience↗

bioRxiv2016

Estimating the implicit component of visuomotor rotation learning by constraining movement preparation time.

When sensory feedback is perturbed, accurate movement is restored by a combination of implicit processes and deliberate re-aiming to strategically compensate for errors. Here, we directly compare two methods used previously to dissociate implicit from explicit learning on a trial-by-trial basis: 1) asking participants to report the direction that they aim their movements, and contrasting this with the directions of the target and the movement that they actually produce, 2) manipulating movement preparation time. By instructing participants to re-aim without a sensory perturbation, we show that re-aiming is possible even with the shortest possible preparation times, particularly when targets are narrowly distributed. Nonetheless, re-aiming is effortful and comes at the cost of increased variability, so we tested whether constraining preparation time is sufficient to suppress strategic re-aiming during adaptation to visuomotor rotation with a broad target distribution. The rate and extent of error reduction under preparation time constraints were similar to estimates of implicit learning obtained from self-report without time pressure, suggesting that participants chose not to apply a re-aiming strategy to correct visual errors under time pressure. Surprisingly, participants who reported aiming directions showed less implicit learning according to an alternative measure, obtained during trials performed without visual feedback. This suggests that the process of reporting can affect the extent or persistence of implicit learning. The data extend existing evidence that restricting preparation time can suppress explicit re-aiming, and provide an estimate of implicit visuomotor rotation learning that does not require participants to report their aiming directions.\n\nNew and NoteworthyDuring sensorimotor adaptation, implicit, error-driven learning can be isolated from explicit strategy-driven re-aiming by subtracting self-reported aiming directions from movement directions, or by restricting movement preparation time. Here, we compared the two methods. Restricting preparation times did not eliminate re-aiming, but was sufficient to suppress reaiming during adaptation with widely-distributed targets. The self-report method produced a discrepancy in implicit learning estimated by subtracting aiming directions, and implicit learning measured in no-feedback trials.

neuroscience↗