Daniel Goldreich

Tactile Acuity is Enhanced in Blindness

Functional imaging studies in blind subjects have shown tactile activation of cortical areas that normally subserve vision, but whether blind people have enhanced tactile acuity has long been controversial. We compared the passive tactile acuity of blind and sighted subjects on a fully automated grating orientation task and used multivariate Bayesian data analysis to determine predictors of acuity. Acuity was significantly superior in blind subjects, independently of the degree of childhood vision, light perception level, or Braille reading. Acuity was strongly dependent on the force of contact between the stimulus surface and the skin, declined with subject age, and was better in women than in men. Despite large intragroup variability, the difference between blind and sighted subjects was highly significant: the average blind subject had the acuity of an average sighted subject of the same gender but 23 years younger. The results suggest that crossmodal plasticity may underlie tactile acuity enhancement in blindness.

Tactile Spatial Acuity Enhancement in Blindness: Evidence for Experience-Dependent Mechanisms

Tactile spatial acuity is enhanced in blindness, according to several studies, but the cause of this enhancement has been controversial. Two competing hypotheses are the tactile experience hypothesis (reliance on the sense of touch drives tactile-acuity enhancement) and the visual deprivation hypothesis (the absence of vision itself drives tactile-acuity enhancement). Here, we performed experiments to distinguish between these two hypotheses. We used force-controlled grating orientation tasks to compare the passive (finger stationary) tactile spatial acuity of 28 profoundly blind and 55 normally sighted humans on the index, middle, and ring fingers of each hand, and on the lips. The tactile experience hypothesis predicted that blind participants would outperform the sighted on the fingers, and that Braille reading would correlate with tactile acuity. The visual deprivation hypothesis predicted that blind participants would outperform the sighted on fingers and lips. Consistent with the tactile experience hypothesis, the blind significantly outperformed the sighted on all fingers, but not on the lips. Additionally, among blind participants, proficient Braille readers on their preferred reading index finger outperformed nonreaders. Finally, proficient Braille readers performed better with their preferred reading index finger than with the opposite index finger, and their acuity on the preferred reading finger correlated with their weekly reading time. These results clearly implicate reliance on the sense of touch as the trigger for tactile spatial acuity enhancement in the blind, and suggest the action of underlying experience-dependent neural mechanisms such as somatosensory and/or cross-modal cortical plasticity.

Texture discrimination and unit recordings in the rat whisker/barrel system

We have developed a semi-automated technique for acquiring neurophysiological data during whisker-based tactile discriminative behavior. Water-deprived, blindfolded rats are tethered by means of a harness vest that permits them to contact a rough (250 micrometer grooves) or smooth discriminandum with only their vibrissae. Discriminanda are mounted on a motor-driven carousel, and the rat indicates its choice (rough, smooth) by licking either a right or left water port located near the carousel. A narrow light beam detects general proximity of the animals nose to the discriminandum, although actual whisker contact is monitored by a SuperVHS camera and measured offline using field-by-field videographic analysis. Rats can be trained within 3-6 weeks at which time they perform 100-150 trials/day at a level of 80% correct. Unit recording from the somatosensory cortex reveals that neurons increase their firing upon whisker contact of a discriminandum and that firing remains elevated during several hundred milliseconds of ongoing contact, even with the smooth surface. Nevertheless, despite the animals ability to distinguish the rough and smooth surfaces, overall neuronal firing rates were indistinguishable for the two surfaces. In some cases, temporal firing patterns differed, although not in a consistent way across recording sites.

Performance of blind and sighted humans on a tactile grating detection task.

We compared the abilities of blind and sighted humans to distinguish grooved from smooth surfaces pressed against the stationary index fingertip. Ranging in age from 20 to 72 years, 37 blind and 47 sighted subjects participated in an automated two-alternative forced-choice tactile grating detection task. The tactile acuity of blind and sighted subjects declined with age at equivalent rates (0.011-mm threshold increase per year), but the blind subjects were able to perceive significantly thinner grooves than were their sighted peers (the average difference between blind and sighted subjects of the same age and gender was 0.267 mm). The blind Braille readers performed no better than the blind nonreaders, and the congenitally blind subjects performed equivalently to those with adult-onset blindness. The superior tactile acuity of blind persons may result from the involvement of normally visually responsive cerebrocortical areas in tactile processing, as shown by functional-imaging studies.

A Bayesian Perceptual Model Replicates the Cutaneous Rabbit and Other Tactile Spatiotemporal Illusions

Background When brief stimuli contact the skin in rapid succession at two or more locations, perception strikingly shrinks the intervening distance, and expands the elapsed time, between consecutive events. The origins of these perceptual space-time distortions are unknown. Methodology/Principal Findings Here I show that these illusory effects, which I term perceptual length contraction and time dilation, are emergent properties of a Bayesian observer model that incorporates prior expectation for speed. Rapidly moving stimuli violate expectation, provoking perceptual length contraction and time dilation. The Bayesian observer replicates the cutaneous rabbit illusion, the tau effect, the kappa effect, and other spatiotemporal illusions. Additionally, it shows realistic tactile temporal order judgment and spatial attention effects. Conclusions/Significance The remarkable explanatory power of this simple model supports the hypothesis, first proposed by Helmholtz, that the brain biases perception in favor of expectation. Specifically, the results suggest that the brain automatically incorporates prior expectation for speed in order to overcome spatial and temporal imprecision inherent in the sensorineural signal.

Two-Point Orientation Discrimination Versus the Traditional Two-Point Test for Tactile Spatial Acuity Assessment

Two-point discrimination is widely used to measure tactile spatial acuity. The validity of the two-point threshold as a spatial acuity measure rests on the assumption that two points can be distinguished from one only when the two points are sufficiently separated to evoke spatially distinguishable foci of neural activity. However, some previous research has challenged this view, suggesting instead that two-point task performance benefits from an unintended non-spatial cue, allowing spuriously good performance at small tip separations. We compared the traditional two-point task to an equally convenient alternative task in which participants attempt to discern the orientation (vertical or horizontal) of two points of contact. We used precision digital readout calipers to administer two-interval forced-choice versions of both tasks to 24 neurologically healthy adults, on the fingertip, finger base, palm, and forearm. We used Bayesian adaptive testing to estimate the participants’ psychometric functions on the two tasks. Traditional two-point performance remained significantly above chance levels even at zero point separation. In contrast, two-point orientation discrimination approached chance as point separation approached zero, as expected for a valid measure of tactile spatial acuity. Traditional two-point performance was so inflated at small point separations that 75%-correct thresholds could be determined on all tested sites for fewer than half of participants. The 95%-correct thresholds on the two tasks were similar, and correlated with receptive field spacing. In keeping with previous critiques, we conclude that the traditional two-point task provides an unintended non-spatial cue, resulting in spuriously good performance at small spatial separations. Unlike two-point discrimination, two-point orientation discrimination rigorously measures tactile spatial acuity. We recommend the use of two-point orientation discrimination for neurological assessment.

Vibrotactile masking experiments reveal accelerated somatosensory processing in congenitally blind Braille readers

Braille reading is a demanding task that requires the identification of rapidly varying tactile patterns. During proficient reading, neighboring characters impact the fingertip at ∼100 ms intervals, and adjacent raised dots within a character at 50 ms intervals. Because the brain requires time to interpret afferent sensorineural activity, among other reasons, tactile stimuli separated by such short temporal intervals pose a challenge to perception. How, then, do proficient Braille readers successfully interpret inputs arising from their fingertips at such rapid rates? We hypothesized that somatosensory perceptual consolidation occurs more rapidly in proficient Braille readers. If so, Braille readers should outperform sighted participants on masking tasks, which demand rapid perceptual processing, but would not necessarily outperform the sighted on tests of simple vibrotactile sensitivity. To investigate, we conducted two-interval forced-choice vibrotactile detection, amplitude discrimination, and masking tasks on the index fingertips of 89 sighted and 57 profoundly blind humans. Sighted and blind participants had similar unmasked detection (25 ms target tap) and amplitude discrimination (compared with 100 μm reference tap) thresholds, but congenitally blind Braille readers, the fastest readers among the blind participants, exhibited significantly less masking than the sighted (masker, 50 Hz, 50 μm; target–masker delays, ±50 and ±100 ms). Indeed, Braille reading speed correlated significantly and specifically with masking task performance, and in particular with the backward masking decay time constant. We conclude that vibrotactile sensitivity is unchanged but that perceptual processing is accelerated in congenitally blind Braille readers.

Prediction, Postdiction, and Perceptual Length Contraction: A Bayesian Low-Speed Prior Captures the Cutaneous Rabbit and Related Illusions

Illusions provide a window into the brain’s perceptual strategies. In certain illusions, an ostensibly task-irrelevant variable influences perception. For example, in touch as in audition and vision, the perceived distance between successive punctate stimuli reflects not only the actual distance but curiously the inter-stimulus time. Stimuli presented at different positions in rapid succession are drawn perceptually toward one another. This effect manifests in several illusions, among them the startling cutaneous rabbit, in which taps delivered to as few as two skin positions appear to hop progressively from one position to the next, landing in the process on intervening areas that were never stimulated. Here we provide an accessible step-by-step exposition of a Bayesian perceptual model that replicates the rabbit and related illusions. The Bayesian observer optimally joins uncertain estimates of spatial location with the expectation that stimuli tend to move slowly. We speculate that this expectation – a Bayesian prior – represents the statistics of naturally occurring stimuli, learned by humans through sensory experience. In its simplest form, the model contains a single free parameter, tau: a time constant for space perception. We show that the Bayesian observer incorporates both pre- and post-dictive inference. Directed spatial attention affects the prediction-postdiction balance, shifting the model’s percept toward the attended location, as observed experimentally in humans. Applying the model to the perception of multi-tap sequences, we show that the low-speed prior fits perception better than an alternative, low-acceleration prior. We discuss the applicability of our model to related tactile, visual, and auditory illusions. To facilitate future model-driven experimental studies, we present a convenient freeware computer program that implements the Bayesian observer; we invite investigators to use this program to create their own testable predictions.

Short-Term Visual Deprivation Does Not Enhance Passive Tactile Spatial Acuity

An important unresolved question in sensory neuroscience is whether, and if so with what time course, tactile perception is enhanced by visual deprivation. In three experiments involving 158 normally sighted human participants, we assessed whether tactile spatial acuity improves with short-term visual deprivation over periods ranging from under 10 to over 110 minutes. We used an automated, precisely controlled two-interval forced-choice grating orientation task to assess each participants ability to discern the orientation of square-wave gratings pressed against the stationary index finger pad of the dominant hand. A two-down one-up staircase (Experiment 1) or a Bayesian adaptive procedure (Experiments 2 and 3) was used to determine the groove width of the grating whose orientation each participant could reliably discriminate. The experiments consistently showed that tactile grating orientation discrimination does not improve with short-term visual deprivation. In fact, we found that tactile performance degraded slightly but significantly upon a brief period of visual deprivation (Experiment 1) and did not improve over periods of up to 110 minutes of deprivation (Experiments 2 and 3). The results additionally showed that grating orientation discrimination tends to improve upon repeated testing, and confirmed that women significantly outperform men on the grating orientation task. We conclude that, contrary to two recent reports but consistent with an earlier literature, passive tactile spatial acuity is not enhanced by short-term visual deprivation. Our findings have important theoretical and practical implications. On the theoretical side, the findings set limits on the time course over which neural mechanisms such as crossmodal plasticity may operate to drive sensory changes; on the practical side, the findings suggest that researchers who compare tactile acuity of blind and sighted participants should not blindfold the sighted participants.

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.