Ryan M. Peters

Gain and phase of perceived virtual rotation evoked by electrical vestibular stimuli

Galvanic vestibular stimulation (GVS) evokes a perception of rotation; however, very few quantitative data exist on the matter. We performed psychophysical experiments on virtual rotations experienced when binaural bipolar electrical stimulation is applied over the mastoids. We also performed analogous real whole body yaw rotation experiments, allowing us to compare the frequency response of vestibular perception with (real) and without (virtual) natural mechanical stimulation of the semicircular canals. To estimate the gain of vestibular perception, we measured direction discrimination thresholds for virtual and real rotations. Real direction discrimination thresholds decreased at higher frequencies, confirming multiple previous studies. Conversely, virtual direction discrimination thresholds increased at higher frequencies, implying low-pass filtering of the virtual perception process occurring potentially anywhere between afferent transduction and cortical responses. To estimate the phase of vestibular perception, participants manually tracked their perceived position during sinusoidal virtual and real kinetic stimulation. For real rotations, perceived velocity was approximately in phase with actual velocity across all frequencies. Perceived virtual velocity was in phase with the GVS waveform at low frequencies (0.05 and 0.1 Hz). As frequency was increased to 1 Hz, the phase of perceived velocity advanced relative to the GVS waveform. Therefore, at low frequencies GVS is interpreted as an angular velocity signal and at higher frequencies GVS becomes interpreted increasingly as an angular position signal. These estimated gain and phase spectra for vestibular perception are a first step toward generating well-controlled virtual vestibular percepts, an endeavor that may reveal the usefulness of GVS in the areas of clinical assessment, neuroprosthetics, and virtual reality.

Tactile Spatial Acuity in Childhood: Effects of Age and Fingertip Size

Tactile acuity is known to decline with age in adults, possibly as the result of receptor loss, but less is understood about how tactile acuity changes during childhood. Previous research from our laboratory has shown that fingertip size influences tactile spatial acuity in young adults: those with larger fingers tend to have poorer acuity, possibly because mechanoreceptors are more sparsely distributed in larger fingers. We hypothesized that a similar relationship would hold among children. If so, children’s tactile spatial acuity might be expected to worsen as their fingertips grow. However, concomitant CNS maturation might result in more efficient perceptual processing, counteracting the effect of fingertip growth on tactile acuity. To investigate, we conducted a cross-sectional study, testing 116 participants ranging in age from 6 to 16 years on a precision-controlled tactile grating orientation task. We measured each participants grating orientation threshold on the dominant index finger, along with physical properties of the fingertip: surface area, volume, sweat pore spacing, and temperature. We found that, as in adults, children with larger fingertips (at a given age) had significantly poorer acuity, yet paradoxically acuity did not worsen significantly with age. We propose that finger growth during development results in a gradual decline in innervation density as receptive fields reposition to cover an expanding skin surface. At the same time, central maturation presumably enhances perceptual processing.

A Tactile Automated Passive-Finger Stimulator (TAPS).

Although tactile spatial acuity tests are used in both neuroscience research and clinical assessment, few automated devices exist for delivering controlled spatially structured stimuli to the skin. Consequently, investigators often apply tactile stimuli manually. Manual stimulus application is time consuming, requires great care and concentration on the part of the investigator, and leaves many stimulus parameters uncontrolled. We describe here a computer-controlled tactile stimulus system, the Tactile Automated Passive-finger Stimulator (TAPS), that applies spatially structured stimuli to the skin, controlling for onset velocity, contact force, and contact duration. TAPS is a versatile, programmable system, capable of efficiently conducting a variety of psychophysical procedures. We describe the components of TAPS, and show how TAPS is used to administer a two-interval forced-choice tactile grating orientation test. Corresponding Author: Daniel Goldreich

Losing touch: age-related changes in plantar skin sensitivity, lower-limb cutaneous reflex strength, and postural stability in older adults.

Age-related changes in the density, morphology, and physiology of plantar cutaneous receptors negatively impact the quality and quantity of balance-relevant information arising from the foot soles. Plantar perceptual sensitivity declines with age and may predict postural instability; however, alteration in lower limb cutaneous reflex strength may also explain greater instability in older adults and has yet to be investigated. We replicated the age-related decline in sensitivity by assessing monofilament and vibrotactile (30 and 250 Hz) detection thresholds near the first metatarsal head bilaterally in healthy young and older adults. We additionally applied continuous 30- and 250-Hz vibration to drive mechanically evoked reflex responses in the tibialis anterior muscle, measured via surface electromyography. To investigate potential relationships between plantar sensitivity, cutaneous reflex strength, and postural stability, we performed posturography in subjects during quiet standing without vision. Anteroposterior and mediolateral postural stability decreased with age, and increases in postural sway amplitude and frequency were significantly correlated with increases in plantar detection thresholds. With 30-Hz vibration, cutaneous reflexes were observed in 95% of young adults but in only 53% of older adults, and reflex gain, coherence, and cumulant density at 30 Hz were lower in older adults. Reflexes were not observed with 250-Hz vibration, suggesting this high-frequency cutaneous input is filtered out by motoneurons innervating tibialis anterior. Our findings have important implications for assessing the risk of balance impairment in older adults.

Older adults demonstrate superior vestibular perception for virtual rotations.

Adult ageing results in a progressive loss of vestibular hair cell receptors and afferent fibres. Given the robustness of vestibulo-ocular and vestibular-evoked whole-body responses to age-related deterioration, it was proposed that the vestibular system compensates centrally. Here we examine the potential for central compensation in vestibular sensitivity with adult ageing by using a combination of real and virtual rotation-based psychophysical testing at two stimulus frequencies (0.1 & 1Hz). Real rotations activate semi-circular canal hair cell receptors naturally via mechanotransduction, while electrical current used to evoke virtual rotations does not rely on mechanical deformation of hair cell receptors to activate vestibular afferents. This two-pronged approach allows us to determine the independent effects of age-related peripheral afferent receptor loss and potential compensatory mechanisms. Older adults had thresholds for discriminating real rotations that were significantly greater than young adults at 0.1Hz (7.2 vs. 3°/s), but the effect of age was weaker (non-significant) at 1Hz (2.4 vs. 1.3°/s). For virtual rotations, older adults had greater thresholds than young adults at 0.1Hz (1.2 vs. 0.5mA), however, older adults outperformed young adults at 1Hz (0.6 vs. 1.1mA). Based on these thresholds, we argue that central vestibular processing gain is enhanced in older adults for 1Hz real and virtual rotations, partially offsetting the negative impact of normal age-related hair cell receptor and primary afferent loss. We propose that the frequency dependence of this compensation reflects the physiological importance of the 1-5Hz range in natural vestibular input.

Tactile orientation perception: an ideal observer analysis of human psychophysical performance in relation to macaque area 3b receptive fields.

The ability to resolve the orientation of edges is crucial to daily tactile and sensorimotor function, yet the means by which edge perception occurs is not well understood. Primate cortical area 3b neurons have diverse receptive field (RF) spatial structures that may participate in edge orientation perception. We evaluated five candidate RF models for macaque area 3b neurons, previously recorded while an oriented bar contacted the monkeys fingertip. We used a Bayesian classifier to assign each neuron a best-fit RF structure. We generated predictions for human performance by implementing an ideal observer that optimally decoded stimulus-evoked spike counts in the model neurons. The ideal observer predicted a saturating reduction in bar orientation discrimination threshold with increasing bar length. We tested 24 humans on an automated, precision-controlled bar orientation discrimination task and observed performance consistent with that predicted. We next queried the ideal observer to discover the RF structure and number of cortical neurons that best matched each participants performance. Human perception was matched with a median of 24 model neurons firing throughout a 1-s period. The 10 lowest-performing participants were fit with RFs lacking inhibitory sidebands, whereas 12 of the 14 higher-performing participants were fit with RFs containing inhibitory sidebands. Participants whose discrimination improved as bar length increased to 10 mm were fit with longer RFs; those who performed well on the 2-mm bar, with narrower RFs. These results suggest plausible RF features and computational strategies underlying tactile spatial perception and may have implications for perceptual learning.

Precise coding of ankle angle and velocity by human calf muscle spindles

Human standing balance control requires the integration of sensory feedback to produce anticipatory, stabilizing ankle torques. However, the ability of human triceps surae muscle spindles to provide reliable sensory feedback regarding the small, slow ankle movements that occur during upright standing has recently come under question. We performed microneurography to directly record axon potentials from single muscle spindle afferents in the human triceps surae during servo-controlled movement of the ankle joint. To simulate movements of the ankle while standing, we delivered random 90-s dorsiflexion/plantar flexion oscillations of the ankle joint, with a peak-to-peak amplitude of 0.7° and frequency content below 0.5Hz. In roughly half of the trials (46%), participants held a low-level, near-isometric contraction of the triceps surae muscles. We demonstrate that afferent activity in a population of muscle spindles closely reflects ankle movements at frequencies and amplitudes characteristic of human standing. Four out of five soleus spindles, and three out of seven gastrocnemius spindles coded for at least a single frequency component of anteroposterior ankle rotation. Concatenating within muscles, coherence was significantly greater for soleus spindles at all stimulus frequencies. Voluntary contraction of the parent muscle reduced spindle sensitivity, but only significantly near the mean power frequency of the stimulus (∼0.3Hz). In conclusion, these results provide direct evidence that triceps surae muscle spindles are potentially capable of providing important sensory feedback for the control of human standing balance.

Cutaneous afferent innervation of the human foot sole: what can we learn from single-unit recordings?

Cutaneous afferents convey exteroceptive information about the interaction of the body with the environment and proprioceptive information about body position and orientation. Four classes of low-threshold mechanoreceptor afferents innervate the foot sole and transmit feedback that facilitates the conscious and reflexive control of standing balance. Experimental manipulation of cutaneous feedback has been shown to alter the control of gait and standing balance. This has led to a growing interest in the design of intervention strategies that enhance cutaneous feedback and improve postural control. The advent of single-unit microneurography has allowed the firing and receptive field characteristics of foot sole cutaneous afferents to be investigated. In this review, we consolidate the available cutaneous afferent microneurographic recordings from the foot sole and provide an analysis of the firing threshold, and receptive field distribution and density of these cutaneous afferents. This work enhances the understanding of the foot sole as a sensory structure and provides a foundation for the continued development of sensory augmentation insoles and other tactile enhancement interventions.

Plantar cutaneous function in Parkinson’s disease patients ON and OFF L-dopa

While Parkinsons disease (PD) is traditionally viewed as a motor disorder, there is mounting evidence that somatosensory function becomes affected as well. However, conflicting reports exist regarding whether plantar sensitivity is reduced in early-onset PD patients. Plantar sensitivity was assessed using monofilaments and a gold-standard, two-interval two-alternative forced choice vibrotactile detection task at both 30 and 250Hz. Lower-limb cutaneous reflexes were assessed by delivering continuous, sinusoidal vibration at 30 and 250Hz while recording muscle activity in Tibialis Anterior. We found no evidence of elevated plantar thresholds or dysfunctional lower-limb cutaneous reflexes in PD patients ON medication. We also found no acute effect of ceasing L-dopa intake on either plantar sensitivity or cutaneous reflexes. Our finding of intact cutaneous function in PD supports the further exploration of therapeutics that enhance plantar sensitivity to minimize postural instability, a source of considerable morbidity in this clinical population.

Frequency characteristics of human muscle and cortical responses evoked by noisy Achilles tendon vibration

Noisy stimuli, along with linear systems analysis, have proven to be effective for mapping functional neural connections. We explored the use of noisy (10-115 Hz) Achilles tendon vibration to examine somatosensory reflexes in the triceps surae muscles in standing healthy young adults (n = 8). We also examined the association between noisy vibration and electrical activity recorded over the sensorimotor cortex using electroencephalography. We applied 2 min of vibration and recorded ongoing muscle activity of the soleus and gastrocnemii using surface electromyography (EMG). Vibration amplitude was varied to characterize reflex scaling and to examine how different stimulus levels affected postural sway. Muscle activity from the soleus and gastrocnemii was significantly correlated with the tendon vibration across a broad frequency range (~10-80 Hz), with a peak located at ~40 Hz. Vibration-EMG coherence positively scaled with stimulus amplitude in all three muscles, with soleus displaying the strongest coupling and steepest scaling. EMG responses lagged the vibration by ~38 ms, a delay that paralleled observed response latencies to tendon taps. Vibration-evoked cortical oscillations were observed at frequencies ~40-70 Hz (peak ~54 Hz) in most subjects, a finding in line with previous reports of sensory-evoked γ-band oscillations. Further examination of the method revealed 1) accurate reflex estimates could be obtained with <60 s of low-level (root mean square = 10 m/s2) vibration; 2) responses did not habituate over 2 min of exposure; and importantly, 3) noisy vibration had a minimal influence on standing balance. Our findings suggest noisy tendon vibration is an effective novel approach to characterize somatosensory reflexes during standing.NEW & NOTEWORTHY We applied noisy (10-115 Hz) vibration to the Achilles tendon to examine the frequency characteristics of lower limb somatosensory reflexes during standing. Ongoing muscle activity was coherent with the noisy vibration (peak coherence ~40 Hz), and coherence positively scaled with increases in stimulus amplitude. Our findings suggest that noisy tendon vibration, along with linear systems analysis, is an effective novel approach to study somatosensory reflex actions in active muscles.