skip to main content


Title: Increase in weighting of vision vs. proprioception associated with force field adaptation
Abstract

Hand position can be estimated by vision and proprioception (position sense). The brain is thought to weight and integrate these percepts to form a multisensory estimate of hand position with which to guide movement. Force field adaptation, a type of cerebellum-dependent motor learning, is associated with both motor and proprioceptive changes. The cerebellum has connections with multisensory parietal regions; however, it is unknown if force adaptation is associated with changes in multisensory perception. If force adaptation affects all relevant sensory modalities similarly, the brain’s weighting of vision vs. proprioception should be maintained. Alternatively, if force perturbation is interpreted as somatosensory unreliability, vision may be up-weighted relative to proprioception. We assessed visuo-proprioceptive weighting with a perceptual estimation task before and after subjects performed straight-ahead reaches grasping a robotic manipulandum. Each subject performed one session with a clockwise or counter-clockwise velocity-dependent force field, and one session in a null field. Subjects increased their weight of vision vs. proprioception in the force field session relative to the null session, regardless of force field direction, in the straight-ahead dimension (F1,44 = 5.13, p = 0.029). This suggests that force field adaptation is associated with an increase in the brain’s weighting of vision vs. proprioception.

 
more » « less
Award ID(s):
1753915
NSF-PAR ID:
10153642
Author(s) / Creator(s):
; ;
Publisher / Repository:
Nature Publishing Group
Date Published:
Journal Name:
Scientific Reports
Volume:
9
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. The brain estimates hand position using vision and position sense (proprioception). The relationship between visual and proprioceptive estimates is somewhat flexible: visual information about the index finger can be spatially displaced from proprioceptive information, resulting in cross-sensory recalibration of the visual and proprioceptive unimodal position estimates. According to the causal inference framework, recalibration occurs when the unimodal estimates are attributed to a common cause and integrated. If separate causes are perceived, then recalibration should be reduced. Here we assessed visuo-proprioceptive recalibration in response to a gradual visuo-proprioceptive mismatch at the left index fingertip. Experiment 1 asked how frequently a 70 mm mismatch is consciously perceived compared to when no mismatch is present, and whether awareness is linked to reduced visuo-proprioceptive recalibration, consistent with causal inference predictions. However, conscious offset awareness occurred rarely. Experiment 2 tested a larger displacement, 140 mm, and asked participants about their perception more frequently, including at 70 mm. Experiment 3 confirmed that participants were unbiased at estimating distances in the 2D virtual reality display. Results suggest that conscious awareness of the mismatch was indeed linked to reduced cross-sensory recalibration as predicted by the causal inference framework, but this was clear only at higher mismatch magnitudes (70–140 mm). At smaller offsets (up to 70 mm), conscious perception of an offset may not override unconscious belief in a common cause, perhaps because the perceived offset magnitude is in range of participants’ natural sensory biases. These findings highlight the interaction of conscious awareness with multisensory processes in hand perception. 
    more » « less
  2. Abstract

    Although multisensory integration is crucial for sensorimotor function, it is unclear how visual and proprioceptive sensory cues are combined in the brain during motor behaviors. Here we characterized the effects of multisensory interactions on local field potential (LFP) activity obtained from the superior parietal lobule (SPL) as non-human primates performed a reaching task with either unimodal (proprioceptive) or bimodal (visual-proprioceptive) sensory feedback. Based on previous analyses of spiking activity, we hypothesized that evoked LFP responses would be tuned to arm location but would be suppressed on bimodal trials, relative to unimodal trials. We also expected to see a substantial number of recording sites with enhanced beta band spectral power for only one set of feedback conditions (e.g. unimodal or bimodal), as was previously observed for spiking activity. We found that evoked activity and beta band power were tuned to arm location at many individual sites, though this tuning often differed between unimodal and bimodal trials. Across the population, both evoked and beta activity were consistent with feedback-dependent tuning to arm location, while beta band activity also showed evidence of response suppression on bimodal trials. The results suggest that multisensory interactions can alter the tuning and gain of arm position-related LFP activity in the SPL.

     
    more » « less
  3. Trial-and-error motor adaptation has been linked to somatosensory plasticity and shifts in proprioception (limb position sense). The role of sensory processing in motor skill learning is less understood. Unlike adaptation, skill learning involves the acquisition of new movement patterns in the absence of perturbation, with performance limited by the speed-accuracy tradeoff. We investigated somatosensory changes during motor skill learning at the behavioral and neurophysiological level. Twenty-eight healthy young adults practiced a maze-tracing task, guiding a robotic manipulandum through an irregular 2D track featuring several abrupt turns. Practice occurred on days 1 and 2. Skill was assessed before practice on day 1 and again on day 3, with learning indicated by a shift in the speed-accuracy function between these assessments. Proprioceptive function was quantified with a passive two-alternative forced choice task. In a subset of 15 participants, we measured short latency afferent inhibition (SAI) to index somatosensory projections to motor cortex. We found that motor practice enhanced the speed-accuracy skill function (F 4,108 = 32.15, p < 0.001) and was associated with improved proprioceptive sensitivity at retention (t 22 = 24.75, p = 0.0031). Further, SAI increased after training (F 1,14 = 5.41, p = 0.036). Interestingly, individuals with larger increases in SAI, reflecting enhanced somatosensory afference to motor cortex, demonstrated larger improvements in motor skill learning. These findings suggest that SAI may be an important functional mechanism for some aspect of motor skill learning. Further research is needed to test what parameters (task complexity, practice time, etc) are specifically linked to somatosensory function. 
    more » « less
  4. Eleni Papageorgiou (Ed.)
    Background

    Research on task performance under visual field loss is often limited due to small and heterogenous samples. Simulations of visual impairments hold the potential to account for many of those challenges. Digitally altered pictures, glasses, and contact lenses with partial occlusions have been used in the past. One of the most promising methods is the use of a gaze-contingent display that occludes parts of the visual field according to the current gaze position. In this study, the gaze-contingent paradigm was implemented in a static driving simulator to simulate visual field loss and to evaluate parallels in the resulting driving and gaze behavior in comparison to patients.

    Methods

    The sample comprised 15 participants without visual impairment. All the subjects performed three drives: with full vision, simulated left-sided homonymous hemianopia, and simulated right-sided homonymous hemianopia, respectively. During each drive, the participants drove through an urban environment where they had to maneuver through intersections by crossing straight ahead, turning left, and turning right.

    Results

    The subjects reported reduced safety and increased workload levels during simulated visual field loss, which was reflected in reduced lane position stability and greater absence of large gaze movements. Initial compensatory strategies could be found concerning a dislocated gaze position and a distorted fixation ratio toward the blind side, which was more pronounced for right-sided visual field loss. During left-sided visual field loss, the participants showed a smaller horizontal range of gaze positions, longer fixation durations, and smaller saccadic amplitudes compared to right-sided homonymous hemianopia and, more distinctively, compared to normal vision.

    Conclusion

    The results largely mirror reports from driving and visual search tasks under simulated and pathological homonymous hemianopia concerning driving and scanning challenges, initially adopted compensatory strategies, and driving safety. This supports the notion that gaze-contingent displays can be a useful addendum to driving simulator research with visual impairments if the results are interpreted considering methodological limitations and inherent differences to the pathological impairment.

     
    more » « less
  5. Baden, Tom (Ed.)
    Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal’s awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes’ undulatory body motions induce reafferent feedback that can encode the body’s instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors’ preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception. 
    more » « less