Proprioception in motor learning: : lessons from a deafferented subject

This document is the Accepted Manuscript version of the following article: N. Yousif, J. Cole, J. Rothwell, and J. Diedrichsen, ‘Proprioception in motor learning: lessons from a deafferented subject’, Experimental Brain Research, Vol. 233 (8): 2449-2459, August 2015. The final publication is available at Springer via https://doi.org/10.1007/s00221-015-4315-8.Proprioceptive information arises from a variety of channels, including muscle, tendon, and skin afferents. It tells us where our static limbs are in space and how they are moving. It remains unclear however, how these proprioceptive modes contribute to motor learning. Here, we studied a subject (IW) who has lost large myelinated fibres below the neck and found that he was strongly impaired in sensing the static position of his upper limbs, when passively moved to an unseen location. When making reaching movements however, his ability to discriminate in which direction the trajectory had been diverted was unimpaired. This dissociation allowed us to test the involvement of static and dynamic proprioception in motor learning. We found that IW showed a preserved ability to adapt to force fields when visual feedback was present. He was even sensitive to the exact form of the force perturbation, responding appropriately to a velocity- or position-dependent force after a single perturbation. The ability to adapt to force fields was also preserved when visual feedback about the lateral perturbation of the hand was withdrawn. In this experiment, however, he did not exhibit a form of use-dependent learning, which was evident in the control participants as a drift of the intended direction of the reaching movement in the perturbed direction. This suggests that this form of learning may depend on static position sense at the end of the movement. Our results indicate that dynamic and static proprioception play dissociable roles in motor learning.Peer reviewedFinal Accepted Versio

Proprioception in motor learning: : lessons from a deafferented subject

This document is the Accepted Manuscript version of the following article: N. Yousif, J. Cole, J. Rothwell, and J. Diedrichsen, ‘Proprioception in motor learning: lessons from a deafferented subject’, Experimental Brain Research, Vol. 233 (8): 2449-2459, August 2015. The final publication is available at Springer via https://doi.org/10.1007/s00221-015-4315-8.Proprioceptive information arises from a variety of channels, including muscle, tendon, and skin afferents. It tells us where our static limbs are in space and how they are moving. It remains unclear however, how these proprioceptive modes contribute to motor learning. Here, we studied a subject (IW) who has lost large myelinated fibres below the neck and found that he was strongly impaired in sensing the static position of his upper limbs, when passively moved to an unseen location. When making reaching movements however, his ability to discriminate in which direction the trajectory had been diverted was unimpaired. This dissociation allowed us to test the involvement of static and dynamic proprioception in motor learning. We found that IW showed a preserved ability to adapt to force fields when visual feedback was present. He was even sensitive to the exact form of the force perturbation, responding appropriately to a velocity- or position-dependent force after a single perturbation. The ability to adapt to force fields was also preserved when visual feedback about the lateral perturbation of the hand was withdrawn. In this experiment, however, he did not exhibit a form of use-dependent learning, which was evident in the control participants as a drift of the intended direction of the reaching movement in the perturbed direction. This suggests that this form of learning may depend on static position sense at the end of the movement. Our results indicate that dynamic and static proprioception play dissociable roles in motor learning.Peer reviewedFinal Accepted Versio

Motor planning brings human primary somatosensory cortex into action-specific preparatory states

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here, we used 7T functional magnetic resonance imaging and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons

Mapping the Integration of Sensory Information across Fingers in Human Sensorimotor Cortex

The integration of somatosensory signals across fingers is essential for dexterous object manipulation. Previous experiments suggest that this integration occurs in neural populations in the primary somatosensory cortex (S1). However, the integration process has not been fully characterized, as previous studies have mainly used 2-finger stimulation paradigms. Here, we addressed this gap by stimulating all 31 single- and multifinger combinations. We measured population-wide activity patterns evoked during finger stimulation in human S1 and primary motor cortex (M1) using 7T fMRI in female and male participants. Using multivariate fMRI analyses, we found clear evidence of unique nonlinear interactions between fingers. In Brodmann area (BA) 3b, interactions predominantly occurred between pairs of neighboring fingers. In BA 2, however, we found equally strong interactions between spatially distant fingers, as well as interactions between finger triplets and quadruplets. We additionally observed strong interactions in the hand area of M1. In both M1 and S1, these nonlinear interactions did not reflect a general suppression of overall activity, suggesting instead that the interactions we observed reflect rich, nonlinear integration of sensory inputs from the fingers. We suggest that this nonlinear finger integration allows for a highly flexible mapping from finger sensory inputs to motor responses that facilitates dexterous object manipulation.SIGNIFICANCE STATEMENT Processing of somatosensory information in primary somatosensory cortex (S1) is essential for dexterous object manipulation. To successfully handle an object, the sensorimotor system needs to detect complex patterns of haptic information, which requires the nonlinear integration of sensory inputs across multiple fingers. Using multivariate fMRI analyses, we characterized brain activity patterns evoked by stimulating all single- and multifinger combinations. We report that progressively stronger multifinger interactions emerge in posterior S1 and in the primary motor cortex (M1), with interactions arising between inputs from neighboring and spatially distant fingers. Our results suggest that S1 and M1 provide the neural substrate necessary to support a flexible mapping from sensory inputs to motor responses of the hand

Variational representational similarity analysis

© 2019 The Authors This technical note describes a variational or Bayesian implementation of representational similarity analysis (RSA) and pattern component modelling (PCM). It considers RSA and PCM as Bayesian model comparison procedures that assess the evidence for stimulus or condition-specific patterns of responses distributed over voxels or channels. On this view, one can use standard variational inference procedures to quantify the contributions of particular patterns to the data, by evaluating second-order parameters or hyperparameters. Crucially, this allows one to use parametric empirical Bayes (PEB) to infer which patterns are consistent among subjects. At the between-subject level, one can then assess the evidence for different (combinations of) hypotheses about condition-specific effects using Bayesian model comparison. Alternatively, one can select a single hypothesis that best explains the pattern of responses using Bayesian model selection. This note rehearses the technical aspects of within and between-subject RSA using a worked example, as implemented in the Statistical Parametric Mapping (SPM) software. En route, we highlight the connection between univariate and multivariate analyses of neuroimaging data and the sorts of analyses that are possible using component modelling and representational similarity analysis

Sign and speech share partially overlapping conceptual representations

Conceptual knowledge is fundamental to human cognition. Yet the extent to which it is influenced by language is unclear. Studies of semantic processing show that similar neural patterns are evoked by the same concepts presented in different modalities (e.g. spoken words and pictures or text) [1–3]. This suggests that conceptual representations are ‘modality independent’. However, an alternative possibility is that the similarity reflects retrieval of common spoken language representations. Indeed, in hearing spoken language users, text and spoken language are co-dependent [4,5] and pictures are encoded via visual and verbal routes [6]. A parallel approach investigating semantic cognition, shows that bilinguals activate similar patterns for the same words in their different languages [7,8]. This suggests that conceptual representations are ‘language independent’. However, this has only been tested in spoken language bilinguals. If different languages evoke different conceptual representations, this should be most apparent comparing languages that differ greatly in structure. Hearing people with signing deaf parents are bilingual in sign and speech: languages conveyed in different modalities. Here we test the influence of modality and bilingualism on conceptual representation by comparing semantic representations elicited by spoken British English and British Sign Language in hearing early, sign-speech bilinguals. We show that representations of semantic categories are shared for sign and speech, but not for individual spoken words and signs. This provides evidence for partially shared representations for sign and speech, and shows that language acts as a subtle filter through which we understand and interact with the world

The planning horizon for movement sequences

When performing a long chain of actions in rapid sequence, future movements need to be planned concur-rently with ongoing action. However, how far ahead we plan, and whether this ability improves with practice, is currently unknown. Here, we designed an experiment in which healthy volunteers produced sequences of 14 finger presses quickly and accurately on a keyboard in response to numerical stimuli. On every trial, participants were only shown a fixed number of stimuli ahead of the current keypress. The size of this viewing window varied between 1 (next digit revealed with the pressing of the current key) and 14 (full view of the sequence). Participants practiced the task for 5 days, and their performance was continuously assessed on random sequences. Our results indicate that participants used the available visual information to plan multiple actions into the future, but that the planning horizon was limited: receiving information about more than three movements ahead did not result in faster sequence production. Over the course of practice, we found larger performance improvements for larger viewing windows and an expansion of the planning horizon. These find-ings suggest that the ability to plan future responses during ongoing movement constitutes an important as-pect of skillful movement. Based on the results, we propose a framework to investigate the neuronal processes underlying simultaneous planning and execution

Flexible switching of feedback control mechanisms allows for learning of different task dynamics.

To produce skilled movements, the brain flexibly adapts to different task requirements and movement contexts. Two core abilities underlie this flexibility. First, depending on the task, the motor system must rapidly switch the way it produces motor commands and how it corrects movements online, i.e. it switches between different (feedback) control policies. Second, it must also adapt to environmental changes for different tasks separately. Here we show these two abilities are related. In a bimanual movement task, we show that participants can switch on a movement-by-movement basis between two feedback control policies, depending only on a static visual cue. When this cue indicates that the hands control separate objects, reactions to force field perturbations of each arm are purely unilateral. In contrast, when the visual cue indicates a commonly controlled object, reactions are shared across hands. Participants are also able to learn different force fields associated with a visual cue. This is however only the case when the visual cue is associated with different feedback control policies. These results indicate that when the motor system can flexibly switch between different control policies, it is also able to adapt separately to the dynamics of different environmental contexts. In contrast, visual cues that are not associated with different control policies are not effective for learning different task dynamics

Body Composition, Protein Deposition, and Efficiency of Lysine Utilization of Growing Pigs Fed Crystalline or Protein-Bound Lysine

Two 4-week experiments were conducted to determine body composition and lysine utilization for protein deposition (PD) in barrows and gilts. Thirty-two growing pigs (16 barrows and 16 gilts; average initial body weight of 40.4 lb) were used in each experiment. Pigs were randomly allotted to one of seven dietary treatments. Four pigs (two barrows and two gilts) were killed at the start and the remaining pigs were killed at the end of the experiments to determine body composition. There were two replications per treatment in each experiment for a total of four replications. Dietary treatments consisted of a basal diet (0.55% lysine) and diets containing 0.65, 0.75, and 0.85% lysine that were achieved by adding lysine to the basal diet from either soybean meal (SBM) or L-lysine•HCl (crystalline). Body protein concentration was greater (P \u3c 0.01) in pigs fed the 0.75% crystalline- supplemented diet than in pigs fed SBM at the same concentration. Gilts had greater (P = 0.05) body lysine concentration than barrows. Body PD and lysine deposition increased linearly with dietary lysine concentration (P \u3c 0.01), but were not different between the two sources of lysine (SBM vs crystalline, respectively) at the same concentration. Barrows and gilts had similar PD and lysine deposition. Body fat concentration decreased (P \u3c 0.01) as the dietary lysine concentration increased for both lysine sources; however, fat deposition was not affected by diet. Water deposition increased with dietary lysine concentration (P = 0.05). Body ash content was similar in pigs fed crystalline or SBM-lysine. The results suggest that PD of growing pigs fed lysine from SBM is similar to that of pigs fed crystalline lysine. Pigs fed 0.75% or 0.85% total lysine (0.20% or 0.30% from SBM) had greater (P \u3c 0.05) efficiency of lysine utilization than pigs fed crystalline-supplemented diets at the same concentration. Gilts utilized lysine from SBM more efficiently than barrows (P \u3c 0.05) at the dietary lysine concentration of 0.75 and 0.85%. The results indicate no significant differences in PD of pigs fed supplemented diets from L-lysine•HCl and soybean meal. However, it appears that the efficiency of lysine utilization of gilts fed diets supplemented with SBM-bound lysine is greater than that of barrows. Supplementing low-protein diets with crystalline amino acids at adequate concentrations can offer environmental benefits towards reducing nitrogen excretion without affecting protein deposition

Body Composition, Protein Deposition, and Efficiency of Lysine Utilization of Growing Pigs Fed Crystalline or Protein-Bound Lysine

Two 4-week experiments were conducted to determine body composition and lysine utilization for protein deposition (PD) in barrows and gilts. Thirty-two growing pigs (16 barrows and 16 gilts; average initial body weight of 40.4 lb) were used in each experiment. Pigs were randomly allotted to one of seven dietary treatments. Four pigs (two barrows and two gilts) were killed at the start and the remaining pigs were killed at the end of the experiments to determine body composition. There were two replications per treatment in each experiment for a total of four replications. Dietary treatments consisted of a basal diet (0.55% lysine) and diets containing 0.65, 0.75, and 0.85% lysine that were achieved by adding lysine to the basal diet from either soybean meal (SBM) or L-lysine•HCl (crystalline). Body protein concentration was greater (P \u3c 0.01) in pigs fed the 0.75% crystalline- supplemented diet than in pigs fed SBM at the same concentration. Gilts had greater (P = 0.05) body lysine concentration than barrows. Body PD and lysine deposition increased linearly with dietary lysine concentration (P \u3c 0.01), but were not different between the two sources of lysine (SBM vs crystalline, respectively) at the same concentration. Barrows and gilts had similar PD and lysine deposition. Body fat concentration decreased (P \u3c 0.01) as the dietary lysine concentration increased for both lysine sources; however, fat deposition was not affected by diet. Water deposition increased with dietary lysine concentration (P = 0.05). Body ash content was similar in pigs fed crystalline or SBM-lysine. The results suggest that PD of growing pigs fed lysine from SBM is similar to that of pigs fed crystalline lysine. Pigs fed 0.75% or 0.85% total lysine (0.20% or 0.30% from SBM) had greater (P \u3c 0.05) efficiency of lysine utilization than pigs fed crystalline-supplemented diets at the same concentration. Gilts utilized lysine from SBM more efficiently than barrows (P \u3c 0.05) at the dietary lysine concentration of 0.75 and 0.85%. The results indicate no significant differences in PD of pigs fed supplemented diets from L-lysine•HCl and soybean meal. However, it appears that the efficiency of lysine utilization of gilts fed diets supplemented with SBM-bound lysine is greater than that of barrows. Supplementing low-protein diets with crystalline amino acids at adequate concentrations can offer environmental benefits towards reducing nitrogen excretion without affecting protein deposition