ABSTRACT
It is unclear how explicit knowledge of an externally imposed mismatch between visual and proprioceptive cues of hand position affects perceptual recalibration. The Bayesian causal inference framework might suggest such knowledge should abolish the visual and proprioceptive recalibration that occurs when individuals perceive these cues as coming from the same source (their hand), while the visuomotor adaptation literature suggests explicit knowledge of a cue conflict does not eliminate implicit compensatory processes. Here we compared visual and proprioceptive recalibration in three groups with varying levels of knowledge about the visuo-proprioceptive cue conflict. All participants estimated the position of visual, proprioceptive, or combined targets related to their left index fingertip, with a 70 mm visuo-proprioceptive offset gradually imposed. Groups 1, 2, and 3 received no information, medium information, and high information, respectively, about the offset. Information was manipulated using instructional and visual cues. All groups performed the task similarly at baseline in terms of variance, weighting, and integration. Results suggest the three groups recalibrated vision and proprioception differently, but there was no difference in variance or weighting. Participants who received only instructional cues about the mismatch (Group 2) did not recalibrate less, on average, than participants provided no information about the mismatch (Group 1). However, participants provided instructional cues and extra visual cues of their hands during the perturbation (Group 3) demonstrated significantly less recalibration than other groups. These findings are consistent with the idea that instructional cues alone are insufficient to override participants' intrinsic belief in common cause and reduce recalibration.
Subject(s)
Cues , Proprioception , Psychomotor Performance , Visual Perception , Humans , Male , Female , Proprioception/physiology , Young Adult , Visual Perception/physiology , Adult , Psychomotor Performance/physiology , Conflict, Psychological , AdolescentABSTRACT
We estimate our hand's position by combining relevant visual and proprioceptive cues. A cross-sensory spatial mismatch can be created by viewing the hand through a prism or, more recently, rotating a visual cursor that represents hand position. This is often done in the context of target-directed reaching to study motor adaptation, the systematic updating of motor commands in response to a systematic movement error. However, a visuo-proprioceptive mismatch also elicits recalibration in the relationship between the hand's seen and felt position. The principles governing visuo-proprioceptive recalibration are poorly understood, compared to motor adaptation. For example, motor adaptation occurs robustly whether the cursor is rotated quickly or slowly, although the former may involve more explicit processes. Here, we asked whether visuo-proprioceptive recalibration, in the absence of motor adaptation, works the same way. Three groups experienced a 70 mm visuo-proprioceptive mismatch about their hand at a Slow, Medium, or Fast rate (0.84, 1.67, or 3.34 mm every two trials, respectively), with no error feedback. Once attained, the 70 mm mismatch was maintained for the remaining trials. Total recalibration differed significantly across groups, with the Fast, Medium, and Slow groups recalibrating 63.7, 56.3, and 42.8 mm on average, respectively. This suggests a slower mismatch rate may be less effective at eliciting recalibration. In contrast to motor adaptation studies, no further recalibration was observed in the maintenance phase. This may be related to the distinct mechanisms thought to contribute to perceptual recalibration via cross-sensory cue conflict versus sensory prediction errors.
Subject(s)
Feedback, Sensory , Psychomotor Performance , Humans , Psychomotor Performance/physiology , Feedback, Sensory/physiology , Proprioception/physiology , Hand/physiology , Adaptation, Physiological/physiology , Perception , Visual Perception/physiologyABSTRACT
Spatial perception of our hand is closely linked to our ability to move the hand accurately. We might therefore expect that reach planning would take into account any changes in perceived hand position; in other words, that perception and action relating to the hand should depend on a common sensorimotor map. However, there is evidence to suggest that changes in perceived hand position affect a body representation that functions separately from the body representation used to control movement. Here, we examined target-directed reaching before and after participants either did (Mismatch group) or did not (Veridical group) experience a cue conflict known to elicit recalibration in perceived hand position. For the reaching task, participants grasped a robotic manipulandum that positioned their unseen hand for each trial. Participants then briskly moved the handle straight ahead to a visual target, receiving no performance feedback. For the perceptual calibration task, participants estimated the locations of visual, proprioceptive, or combined cues about their unseen hand. The Mismatch group experienced a gradual 70-mm forward mismatch between visual and proprioceptive cues, resulting in forward proprioceptive recalibration. Participants made significantly shorter reaches after this manipulation, consistent with feeling their hand to be further forward than it was, but reaching performance returned to baseline levels after only 10 reaches. The Veridical group, after exposure to veridically aligned visual and proprioceptive cues about the hand, showed no change in reach distance. These results suggest that perceptual recalibration affects the same sensorimotor map that is used to plan target-directed reaches.NEW & NOTEWORTHY If perceived hand position changes, we might assume this affects the sensorimotor map and, in turn, reaches made with that hand. However, there is evidence for separate body representations involved in perception versus action. After a cross-sensory conflict that results in proprioceptive recalibration in the forward direction, participants made shorter reaches as predicted, but only briefly. This suggests perceptual recalibration does affect the sensorimotor map used to plan reaches, but the interaction may be short-lived.
Subject(s)
Psychomotor Performance , Visual Perception , Humans , Adaptation, Physiological , Feedback, Sensory , Hand , ProprioceptionABSTRACT
The brain estimates hand position using visual and proprioceptive cues, which are combined to give an integrated multisensory estimate. Spatial mismatches between cues elicit recalibration, a compensatory process where each unimodal estimate is shifted closer to the other. It is unclear how well visuo-proprioceptive recalibration is retained after mismatch exposure. Here we asked whether direct vision and/or active movement of the hand can undo visuo-proprioceptive recalibration, and whether recalibration is still evident 24 h later. 75 participants performed two blocks of visual, proprioceptive, and combination trials, with no feedback or direct vision of the hand. In Block 1, a 70 mm visuo-proprioceptive mismatch was gradually imposed, and recalibration assessed. Block 2 tested retention. Between blocks, Groups 1-4 rested or made active movements with their directly visible or unseen hand for several minutes. Group 5 had a 24-h gap between blocks. All five groups recalibrated both vision and proprioception in Block 1, and Groups 1-4 retained most of this recalibration in Block 2. Interestingly, Group 5 showed an offline increase in proprioceptive recalibration, but retained little visual recalibration. Our results suggested that visuo-proprioceptive recalibration is robustly retained in the short-term. In the longer term, contextual factors may affect retention.
Subject(s)
Adaptation, Physiological , Psychomotor Performance , Humans , Feedback, Sensory , Proprioception , Hand , Visual PerceptionABSTRACT
Finger position sense is a proprioceptive modality highly important for fine motor control. Its developmental time course is largely unknown. This cross-sectional study examined its typical development in 138 children (8-17 years) and a group of 14 healthy young adults using a fast and novel psychophysical test that yielded objective measures of position sense acuity. Participants placed their hands underneath a computer tablet and judged the perceived position of their unseen index finger relative to two visible areas displayed on a tablet following a two-forced-choice paradigm. Responses were fitted to a psychometric acuity function from which the difference between the point-of-subjective-equality and the veridical finger position (ΔPSE) was derived as a measure of position sense bias, and the uncertainty area (UA) as a measure of precision. The main results are: First, children under 12 exhibited a significantly greater UA than adults while adolescent children (13-17 years) exhibited no significant differences when compared to adults. Second, no significant age-related differences in ΔPSE were found across the age range of 8-17 years. This implies that the typical development of finger position sense from late childhood to adulthood is characterized as an age-dependent increase in proprioceptive precision and not as a decrease in bias.
Subject(s)
Fingers , Upper Extremity , Young Adult , Humans , Child , Adolescent , Cross-Sectional Studies , Fingers/physiology , Upper Extremity/physiology , Proprioception/physiology , HandABSTRACT
Recent investigations have identified water polo athletes as at risk for concussions and repetitive subconcussive head impacts. Head impact exposure in collegiate varsity women's water polo, however, has not yet been longitudinally quantified. We aimed to determine the relationship between cumulative and acute head impact exposure across pre-season training and changes in serum biomarkers of brain injury. Twenty-two Division I collegiate women's water polo players were included in this prospective observational study. They wore sensor-installed mouthguards during all practices and scrimmages during eight weeks of pre-season training. Serum samples were collected at six time points (at baseline, before and after scrimmages during weeks 4 and 7, and after the eight-week pre-season training period) and assayed for neurofilament light (NfL) and glial fibrillary acidic protein (GFAP) using Simoa® Human Neurology 2-Plex B assay kits. Serum GFAP increased over time (e.g., an increase of 0.6559 pg/mL per week; p = 0.0087). Neither longitudinal nor acute pre-post scrimmage changes in GFAP, however, were associated with head impact exposure. Contrarily, an increase in serum NfL across the study period was associated with cumulative head impact magnitude (sum of peak linear acceleration: B = 0.015, SE = 0.006, p = 0.016; sum of peak rotational acceleration: B = 0.148, SE = 0.048, p = 0.006). Acute changes in serum NfL were not associated with head impacts recorded during the two selected scrimmages. Hormonal contraceptive use was associated with lower serum NfL and GFAP levels over time, and elevated salivary levels of progesterone were also associated with lower serum NfL levels. These results suggest that detecting increases in serum NfL may be a useful way to monitor cumulative head impact burden in women's contact sports and that female-specific factors, such as hormonal contraceptive use and circulating progesterone levels, may be neuroprotective, warranting further investigations.
Subject(s)
Brain Concussion , Football , Water Sports , Humans , Female , Glial Fibrillary Acidic Protein , Intermediate Filaments , Progesterone , Football/injuries , BiomarkersABSTRACT
Balance relies on several types of sensory information, including somatosensory senses such as touch and position sense (proprioception). As these senses decline in older adults, there is a question of whether shoes limit somatosensory feedback from the floor. Textured insoles are designed to stimulate the soles of the feet to enhance tactile feedback. Textured insoles have shown balance benefits in some populations, but it is unclear if such tactile stimulation improves a person's balance even in cushioned athletic shoes, which dampen proprioceptive signals. Here we ask whether tactile vs. proprioceptive cues contribute differently to balance control in the healthy somatosensory system. We assessed balance in 20 healthy young adults under four footwear conditions: cushioned shoes with regular insoles, cushioned shoes with textured insoles, barefoot, and minimalist shoes. Each condition was evaluated using the Y-Balance Test (YBT) and the Balance Error Scoring System (BESS), validated tests of dynamic and static balance, respectively. YBT is a dynamic reaching test performed on one leg. The BESS includes various stance conditions with eyes closed. The results showed that footwear influenced dynamic balance only, with textured insoles leading to significantly better performance than barefoot and minimalist shoes did in the YBT. These results suggest that at least for dynamic balance, balance benefits of tactile stimulation from the textured insoles offset any dampening of proprioception caused by the athletic shoes' cushioning. Future research on how these conditions compare in older adults may lead to improved footwear recommendations to reduce fall risk and injuries for that population.
Subject(s)
Sports , Touch , Young Adult , Humans , Aged , Lower Extremity , Foot/physiology , Proprioception/physiology , Shoes , Postural Balance/physiologyABSTRACT
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.
ABSTRACT
When visual and proprioceptive estimates of hand position disagree (e.g., viewing the hand underwater), the brain realigns them to reduce mismatch. This perceptual change is reflected in primary motor cortex (M1) excitability, suggesting potential relevance for hand movement. Here, we asked whether fingertip visuo-proprioceptive misalignment affects only the brain's representation of that finger (somatotopically focal), or extends to other parts of the limb that would be needed to move the misaligned finger (somatotopically broad). In Experiments 1 and 2, before and after misaligned or veridical visuo-proprioceptive training at the index finger, we used transcranial magnetic stimulation to assess M1 representation of five hand and arm muscles. The index finger representation showed an association between M1 excitability and visuo-proprioceptive realignment, as did the pinkie finger representation to a lesser extent. Forearm flexors, forearm extensors, and biceps did not show any such relationship. In Experiment 3, participants indicated their proprioceptive estimate of the fingertip, knuckle, wrist, and elbow, before and after misalignment at the fingertip. Proprioceptive realignment at the knuckle, but not the wrist or elbow, was correlated with realignment at the fingertip. These results suggest the effects of visuo-proprioceptive mismatch are somatotopically focal in both sensory and motor domains.
Subject(s)
Proprioception , Transcranial Magnetic Stimulation , Fingers/physiology , Hand , Humans , Movement/physiology , Proprioception/physiologyABSTRACT
BACKGROUND: It is well established that proprioception (position sense) is important for motor control, yet its role in motor learning and associated plasticity is not well understood. We previously demonstrated that motor skill learning is associated with enhanced proprioception and changes in sensorimotor neurophysiology. However, the neural substrates mediating these effects are unclear. OBJECTIVE: To determine whether suppressing activity in the cerebellum and somatosensory cortex (S1) affects proprioceptive changes associated with motor skill learning. METHODS: 54 healthy young adults practiced a skill involving visually-guided 2D reaching movements through an irregular-shaped track using a robotic manipulandum with their right hand. Proprioception was measured using a passive two-alternative choice task before and after motor practice. Continuous theta burst stimulation (cTBS) was delivered over S1 or the cerebellum (CB) at the end of training for two consecutive days. We compared group differences (S1, CB, Sham) in proprioception and motor skill, quantified by a speed-accuracy function, measured on a third consecutive day (retention). RESULTS: As shown previously, the Sham group demonstrated enhanced proprioceptive sensitivity after training and at retention. The S1 group had impaired proprioceptive function at retention through online changes during practice, whereas the CB group demonstrated offline decrements in proprioceptive function. All groups demonstrated motor skill learning. However, the magnitude of learning differed between the CB and Sham groups, consistent with a role for the cerebellum in motor learning. CONCLUSION: Overall, these findings suggest that the cerebellum and S1 are important for distinct aspects of proprioceptive changes during skill learning.
Subject(s)
Motor Skills , Transcranial Magnetic Stimulation , Cerebellum , Humans , Learning , Proprioception , Young AdultABSTRACT
Motor skill learning involves both sensorimotor adaptation (calibrating the response to task dynamics and kinematics), and sequence learning (executing task elements in the correct order at the necessary speed). These processes typically occur together in natural behavior and share much in common, such as working memory demands, development, and possibly neural substrates. However, sensorimotor and sequence learning are usually studied in isolation in research settings, for example as force field adaptation or serial reaction time tasks (SRTT), respectively. It is therefore unclear whether having predictive sequence information during sensorimotor adaptation would facilitate performance, perhaps by improving sensorimotor planning, or if it would impair performance, perhaps by occupying neural resources needed for sensorimotor adaptation. Here we evaluated adaptation to a position-dependent force field in two different SRTT contexts: In Experiment 1, 28 subjects reached between 4 targets in a sequenced or random order. In Experiment 2, 40 subjects reached to one target, but 3 force field directions were applied in a sequenced or random order. No consistent influence of target position sequence on force field adaptation was observed in Experiment 1. However, sequencing of force field directions facilitated sensorimotor adaptation and retention in Experiment 2. This is inconsistent with the idea that sensorimotor and sequence learning share neural resources in any mutually exclusive fashion. These findings indicate that under certain conditions, sequence learning interacts with sensorimotor adaptation in a facilitatory manner. Future research will be needed to determine what circumstances and features of sequence learning are facilitatory to sensorimotor adaptation.
Subject(s)
Adaptation, Physiological/physiology , Biomechanical Phenomena/physiology , Learning/physiology , Psychomotor Performance/physiology , Adult , Humans , Serial Learning/physiology , Young AdultABSTRACT
Recent clinical and neurobehavioral evidence suggests cerebellar dysfunction in schizophrenia (SZ). We used the prism adaptation motor task (PAT) to probe specific cerebellar circuits in the disorder. PAT requires cerebellum-dependent motor adaptation, perceptual remapping, and strategic control. A failure to engage in early corrective processes may indicate impairment within either the cerebellum or regions contributing to strategic components, such as the parietal lobe, while an inability to develop and retain a visuomotor shift with time strongly suggests cerebellar impairment. Thirty-one individuals with SZ and 31 individuals without a history of psychological disorders completed PAT. Subjects reached to a target before, during, and following prism exposure, while their movements were recorded using motion-sensing technology. The SZ group performed worse on conditions consisting of adaptation, post-adaptation, aftereffects, and reorientation, thereby demonstrating a failure to adapt to the same degree as healthy controls. SZ performance remained impaired even with visual feedback and did not differ from controls at baseline, suggesting the observed deficit is specific to adaptation. Results indicate that sensorimotor adaptation is impaired in SZ and implicate disturbances in cerebellar circuits.
ABSTRACT
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 trade-off. We investigated somatosensory changes during motor skill learning at the behavioral and neurophysiological levels. Twenty-eight healthy young adults practiced a maze-tracing task, guiding a robotic manipulandum through an irregular two-dimensional 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 (F4,108 = 32.15, P < 0.001) and was associated with improved proprioceptive sensitivity at retention (t22 = 24.75, P = 0.0031). Furthermore, SAI increased after training (F1,14 = 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.NEW & NOTEWORTHY Somatosensory processing has been implicated in motor adaptation, where performance recovers from a perturbation such as a force field. We investigated somatosensory function during motor skill learning, where a new motor pattern is acquired in the absence of perturbation. After skill practice, we found changes in proprioception and short-latency afferent inhibition (SAI), signifying somatosensory change at both the behavioral and neurophysiological levels. SAI may be an important functional mechanism by which individuals learn motor skills.
Subject(s)
Afferent Pathways/physiology , Learning/physiology , Motor Cortex/physiology , Motor Skills/physiology , Neural Inhibition/physiology , Neuronal Plasticity/physiology , Proprioception/physiology , Adolescent , Adult , Female , Humans , Male , Practice, Psychological , Transcranial Magnetic Stimulation , Young AdultABSTRACT
To control hand movement, we have both vision and proprioception, or position sense. The brain is known to integrate these to reduce variance. Here we ask whether older adults integrate vision and proprioception in a way that minimizes variance as young adults do, and whether older subjects compensate for an imposed visuo-proprioceptive mismatch as young adults do. Ten healthy older adults (mean age 69) and 10 healthy younger adults (mean age 19) participated. Subjects were asked to estimate the position of visual, proprioceptive, and combined targets, with no direct vision of either hand. After a veridical baseline block, a spatial visuo-proprioceptive misalignment was gradually imposed by shifting the visual component forward from the proprioceptive component without the subject's awareness. Older subjects were more variable than young subjects at estimating both visual and proprioceptive target positions. Older subjects tended to rely more heavily on vision than proprioception compared to younger subjects. However, the weighting of vision vs. proprioception was correlated with minimum variance predictions for both older and younger adults, suggesting that variance-minimizing mechanisms are present to some degree in older adults. Visual and proprioceptive realignment were similar for young and older subjects in the misalignment block, suggesting older subjects are able to realign as much as young subjects. These results suggest that intact multisensory processing in older adults should be explored as a potential means of mitigating degradation in individual sensory systems.
Subject(s)
Hand/physiology , Proprioception/physiology , Psychomotor Performance/physiology , Visual Perception/physiology , Adolescent , Age Factors , Aged , Aged, 80 and over , Female , Humans , Male , Middle Aged , Young AdultABSTRACT
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.
Subject(s)
Proprioception/physiology , Vision, Ocular/physiology , Visual Perception/physiology , Acclimatization , Adaptation, Physiological , Adolescent , Adult , Female , Hand/physiology , Humans , Male , Movement , Psychomotor Performance/physiology , Sensorimotor Cortex/physiology , Somatosensory Cortex/physiologyABSTRACT
BACKGROUND AND PURPOSE: Proprioceptive deficits in the hand are common following stroke, but current clinical measurement techniques are too imprecise to detect subtle impairments or small changes. We developed a tablet-based tool to measure static hand proprioception using an adaptive staircase procedure. METHODS: In 16 individuals with chronic stroke and age-matched controls, we quantified proprioception at the metacarpophalangeal joint of the index finger using 3 methods: the tablet task, a custom passive movement direction discrimination test (PMDD), and a manual assessment similar to the Fugl-Meyer (F-M) proprioception subsection. RESULTS: The tablet-based measure and the PMDD both identified impaired proprioception in the affected hand relative to the unaffected hand (P = 0.024 and 0.028), and relative to the control group (P = 0.040 and 0.032), while manual assessment did not. The PMDD had a ceiling effect as movement excursions greater than 15 were not biomechanically feasible. The tablet-based measure and the PMDD detected impaired proprioception in 56% to 75%, and the F-M in only 29%, of patients. PMDD and tablet-based measures were both correlated with primary tactile sensation, but not manual dexterity. DISCUSSION AND CONCLUSIONS: Both the tablet-based tool and the custom PMDD performed better than manual assessment. The PMDD may be useful when the deficit is mild or assessment of dynamic proprioception is desired. As the tablet-based measure does not have the ceiling effect that is associated with the PMDD, it may be useful with any level of proprioceptive impairment, and may be preferable if testing or clinician training time needs to be minimized, or pain or spasticity is present.Video Abstract available for more insights from the authors (see the Video, Supplementary Digital Content 1, available at: http://links.lww.com/JNPT/A256).
Subject(s)
Diagnostic Techniques, Neurological , Fingers/physiopathology , Proprioception/physiology , Sensation Disorders/diagnosis , Sensation Disorders/physiopathology , Stroke/physiopathology , Adult , Aged , Aged, 80 and over , Diagnostic Techniques, Neurological/instrumentation , Female , Humans , Male , Middle Aged , Sensation Disorders/etiology , Stroke/complicationsABSTRACT
When people match an unseen hand to a visual or proprioceptive target, they make both variable and systematic (bias) errors. Variance is a well-established factor in behavior, but the origin and implications of bias, and its connection to variance, are poorly understood. Eighty healthy adults matched their unseen right index finger to proprioceptive (left index finger) and visual targets with no performance feedback. We asked whether matching bias was related to target modality and to the magnitude or spatial properties of matching variance. Bias errors were affected by target modality, with subjects estimating visual and proprioceptive targets 20 mm apart. We found three pieces of evidence to suggest a connection between bias and variable errors: 1) for most subjects, the target modality that yielded greater spatial bias was also estimated with greater variance; 2) magnitudes of matching bias and variance were somewhat correlated for each target modality ( R = 0.24 and 0.29); and 3) bias direction was closely related to the angle of the major axis of the confidence ellipse ( R = 0.60 and 0.63). However, whereas variance was significantly correlated with visuo-proprioceptive weighting as predicted by multisensory integration theory ( R = -0.29 and 0.27 for visual and proprioceptive variance, respectively), bias was not. In a second session, subjects improved their matching variance, but not bias, for both target modalities, indicating a difference in stability. Taken together, these results suggest bias and variance are related only in some respects, which should be considered in the study of multisensory behavior. NEW & NOTEWORTHY People matching visual or proprioceptive targets make both variable and systematic (bias) errors. Multisensory integration is thought to minimize variance, but if the less variable modality has more bias, behavioral accuracy will decrease. Our data set suggests this is unusual. However, although bias and variable errors were spatially related, they differed in both stability and correlation with multisensory weighting. This suggests the bias-variance relationship is not straightforward, and both should be considered in multisensory behavior.
Subject(s)
Fingers/physiology , Proprioception/physiology , Psychomotor Performance/physiology , Space Perception/physiology , Visual Perception/physiology , Adult , Female , Humans , Male , Young AdultABSTRACT
Spatial realignment of visual and proprioceptive estimates of hand position is necessary both to keep the estimates in register over time and to compensate for sensory perturbations. Such realignment affects perceived hand position, which the brain must use to plan hand movements. We would therefore expect visuo-proprioceptive realignment to affect the motor system at some level, but the physiological basis of this interaction is unknown. Here, we asked whether activity in primary motor cortex (M1), a well-known substrate of motor control, shows evidence of change after visuo-proprioceptive realignment. In two sessions each, 32 healthy adults experienced spatially misaligned or veridical visual and proprioceptive information about their static left index finger. Participants indicated perceived finger position with no performance feedback or knowledge of results. Using TMS over the M1 representation of the misaligned finger, we found no average difference between sessions. However, regression analysis indicated that, in the misaligned session only, proprioceptive realignment was linked with a decrease in M1 activity and visual realignment was linked with an increase in M1 activity. Proprioceptive and visual realignment were inversely related to each other. These results suggest that visuo-proprioceptive realignment does indeed have a physiological impact on the motor system. The lack of a between-session mean difference in M1 activity suggests that the basis of the effect is not the multisensory realignment computation itself, independent of modality. Rather, the changes in M1 are consistent with a modality-specific neural mechanism, such as modulation of somatosensory cortex or dorsal stream visual areas that impact M1.