Developmental changes in audiotactile event perception.

The fission and fusion illusions provide measures of multisensory integration. The sound-induced tap fission illusion occurs when a tap is paired with two distractor sounds, resulting in the perception of two taps; the sound-induced tap fusion illusion occurs when two taps are paired with a single sound, resulting in the perception of a single tap. Using these illusions, we measured integration in three groups of children (9-, 11-, and 13-year-olds) and compared them with a group of adults. Based on accuracy, we derived a measure of magnitude of illusion and used a signal detection analysis to estimate perceptual discriminability and decisional criterion. All age groups showed a significant fission illusion, whereas only the three groups of children showed a significant fusion illusion. When compared with adults, the 9-year-olds showed larger fission and fusion illusions (i.e., reduced discriminability and greater bias), whereas the 11-year-olds were adult-like for fission but showed some differences for fusion: significantly worse discriminability and marginally greater magnitude and criterion. The 13-year-olds were adult-like on all measures. Based on the pattern of data, we speculate that the developmental trajectories for fission and fusion differ. We discuss these developmental results in the context of three non-mutually exclusive theoretical frameworks: sensory dominance, maximum likelihood estimation, and causal inference.

The development of audio-visual temporal precision precedes its rapid recalibration.

Through development, multisensory systems reach a balance between stability and flexibility: the systems integrate optimally cross-modal signals from the same events, while remaining adaptive to environmental changes. Is continuous intersensory recalibration required to shape optimal integration mechanisms, or does multisensory integration develop prior to recalibration? Here, we examined the development of multisensory integration and rapid recalibration in the temporal domain by re-analyzing published datasets for audio-visual, audio-tactile, and visual-tactile combinations. Results showed that children reach an adult level of precision in audio-visual simultaneity perception and show the first sign of rapid recalibration at 9 years of age. In contrast, there was very weak rapid recalibration for other cross-modal combinations at all ages, even when adult levels of temporal precision had developed. Thus, the development of audio-visual rapid recalibration appears to require the maturation of temporal precision. It may serve to accommodate distance-dependent travel time differences between light and sound.

Developmental changes in the perception of audiotactile simultaneity.

We charted the developmental trajectory of the perception of audiotactile simultaneity by testing three groups of children (aged 7, 9, and 11 years) and one group of adults. A white noise burst and a tap to the index finger were presented at 1 of 13 stimulus onset asynchronies (SOAs), and the participants were asked to report whether the two stimuli were simultaneous. Compared with adults, 7-year-olds made significantly more simultaneous responses at 9 of the 13 SOAs, whereas 9-year-olds differed from adults at only 2 SOAs. The precision of simultaneity perception was lower, and response errors were higher, in younger children than in adults. The 11-year-olds were adult-like on all measures, thereby demonstrating that judgments about simultaneity for audiotactile stimuli are mature by 11 years. This developmental pattern is similar to that for simultaneity perception for visuotactile stimuli but later than that for audiovisual stimuli. The longer developmental trajectories of the perception of simultaneity between touch and vision and between touch and audition may arise from the need to coordinate and recalibrate between different reference frames and different neural transmission times in each sensory system during body growth; in addition, the ubiquity of audiovisual experience in everyday life may accelerate the development of that modality pairing.

Developmental changes in the perception of visuotactile simultaneity.

A simultaneity judgment (SJ) task was used to measure the developmental trajectory of visuotactile simultaneity perception in children (aged 7, 9, 11, and 13 years) and adults. Participants were presented with a visual flash in the center of a computer monitor and a tap on their right index finger (located 20° below the flash) with 13 possible stimulus onset asynchronies (SOAs). Participants reported whether the flash and tap were presented at the same time. Compared with the adult group, children aged 7 and 9 years made more simultaneous responses when the tap led by more than 300 ms and when the flash led by more than 200 ms, whereas they made fewer simultaneous responses at the 0 ms SOA. Model fitting demonstrated that the window of visuotactile simultaneity became narrower with development and reached adult-like levels between 9 and 11 years of age. Response errors decreased continuously until 11 years of age. The point of subjective simultaneity (PSS) was located on the tactile-leading side in all participants tested, indicating that 7-year olds (the youngest age tested) are adult-like on this measure. In summary, the perception of visuotactile simultaneity is not fully mature until 11 years of age. The protracted development of visuotactile simultaneity perception may be related to the need for crossmodal recalibration as the body grows and to the developmental improvements in the ability to optimally integrate visual and tactile signals.

The relationship between discrimination and memory for spacing and feature changes in houses.

Adults need to discriminate between stimuli and recognize those previously seen. For faces, feature changes (e.g., different eyes) and spacing changes (e.g., distances between eyes) are important cues. In two experiments, we assessed the influence of these on discrimination and recognition of houses, a commonly used control in face studies. In both experiments, discrimination was better for feature than spacing changes. Memory for spacing changes was generally poor but aided by extra learning and intermixing change types. Conversely, memory for features was good, especially when there were few houses, and change type was blocked. Unexpectedly, memory was best for differences that might signal something about occupants (e.g., changes to garden or bins), perhaps akin to hairstyles for faces. Overall, results are consistent with previous work showing poor discrimination of spacing in non-face objects and extends them to show that, unlike for faces, spacing differences are also not well remembered.

Central-peripheral differences in audiovisual and visuotactile event perception.

We examined audiovisual and visuotactile integration in the central and peripheral visual field using visual fission and fusion illusions induced by sounds or taps. The fission illusion occurs when a single flash is perceived as two flashes if paired with two beeps or taps; the fusion illusion, by contrast, occurs when two flashes are perceived as a single flash if the flashes are paired with a single beep or tap. Beeps and taps induced similar patterns of illusions: the fission illusion was larger in the periphery than in the center, whereas the fusion illusion was larger in the center than in the periphery. An analysis based on signal detection theory revealed that both a decline in discriminability and a shift in criterion were associated with the more pronounced fission induced by sounds in the periphery. In contrast, only a shift in criterion was associated with the larger fission induced by taps in the periphery, and the larger fusion induced by a sound or tap in the center. To accommodate these findings, two accounts are proposed: audiovisual signals are more likely to be integrated in peripheral than in central vision, and the interpretation of visual signals favors discontinuous percepts, especially in the periphery.

Electrophysiological evidence of altered visual processing in adults who experienced visual deprivation during infancy.

We examined the role of early visual input in visual system development by testing adults who had been born with dense bilateral cataracts that blocked all patterned visual input during infancy until the cataractous lenses were removed surgically and the eyes fitted with compensatory contact lenses. Patients viewed checkerboards and textures to explore early processing regions (V1, V2), Glass patterns to examine global form processing (V4), and moving stimuli to explore global motion processing (V5). Patients' ERPs differed from those of controls in that (1) the V1 component was much smaller for all but the simplest stimuli and (2) extrastriate components did not differentiate amongst texture stimuli, Glass patterns, or motion stimuli. The results indicate that early visual deprivation contributes to permanent abnormalities at early and mid levels of visual processing, consistent with enduring behavioral deficits in the ability to process complex textures, global form, and global motion.

Early Binocular Input Is Critical for Development of Audiovisual but Not Visuotactile Simultaneity Perception.

Temporal simultaneity provides an essential cue for integrating multisensory signals into a unified perception. Early visual deprivation, in both animals and humans, leads to abnormal neural responses to audiovisual signals in subcortical and cortical areas [1-5]. Behavioral deficits in integrating complex audiovisual stimuli in humans are also observed [6, 7]. It remains unclear whether early visual deprivation affects visuotactile perception similarly to audiovisual perception and whether the consequences for either pairing differ after monocular versus binocular deprivation [8-11]. Here, we evaluated the impact of early visual deprivation on the perception of simultaneity for audiovisual and visuotactile stimuli in humans. We tested patients born with dense cataracts in one or both eyes that blocked all patterned visual input until the cataractous lenses were removed and the affected eyes fitted with compensatory contact lenses (mean duration of deprivation = 4.4 months; range = 0.3-28.8 months). Both monocularly and binocularly deprived patients demonstrated lower precision in judging audiovisual simultaneity. However, qualitatively different outcomes were observed for the two patient groups: the performance of monocularly deprived patients matched that of young children at immature stages, whereas that of binocularly deprived patients did not match any stage in typical development. Surprisingly, patients performed normally in judging visuotactile simultaneity after either monocular or binocular deprivation. Therefore, early binocular input is necessary to develop normal neural substrates for simultaneity perception of visual and auditory events but not visual and tactile events.

The role of early visual input in the development of contour interpolation: the case of subjective contours.

We tested the effect of early monocular and binocular deprivation of normal visual input on the development of contour interpolation. Patients deprived from birth by dense central cataracts in one or both eyes, and age-matched controls, discriminated between fat and thin shapes formed by either illusory or luminance-defined contours. Thresholds indicated the minimum amount of curvature (the fatness or thinness) required for discrimination of the illusory shape, providing a measure of the precision of interpolation. The results show that individuals deprived of visual input in one eye, but not those deprived in both eyes, later show deficits in perceptual interpolation. The deficits were shown mostly for weakly supported contours in which interpolation of contours between the inducers was over a large distance relative to the size of the inducers. Deficits shown for the unilateral but not for the bilateral patients point to the detrimental effect of unequal competition between the eyes for cortical connections on the later development of the mechanisms underlying contour interpolation.

The development of the perception of audiovisual simultaneity.

We measured the typical developmental trajectory of the window of audiovisual simultaneity by testing four age groups of children (5, 7, 9, and 11 years) and adults. We presented a visual flash and an auditory noise burst at various stimulus onset asynchronies (SOAs) and asked participants to report whether the two stimuli were presented at the same time. Compared with adults, children aged 5 and 7 years made more simultaneous responses when the SOAs were beyond ± 200 ms but made fewer simultaneous responses at the 0 ms SOA. The point of subjective simultaneity was located at the visual-leading side, as in adults, by 5 years of age, the youngest age tested. However, the window of audiovisual simultaneity became narrower and response errors decreased with age, reaching adult levels by 9 years of age. Experiment 2 ruled out the possibility that the adult-like performance of 9-year-old children was caused by the testing of a wide range of SOAs. Together, the results demonstrate that the adult-like precision of perceiving audiovisual simultaneity is developed by 9 years of age, the youngest age that has been reported to date.

Motion perception: a review of developmental changes and the role of early visual experience.

Significant controversies have arisen over the developmental trajectory for the perception of global motion. Studies diverge on the age at which it becomes adult-like, with estimates ranging from as young as 3 years to as old as 16. In this article, we review these apparently conflicting results and suggest a potentially unifying hypothesis that may also account for the contradictory literature in neurodevelopmental disorders, such as Autism Spectrum Disorder (ASD). We also discuss the extent to which patterned visual input during this period is necessary for the later development of motion perception. We conclude by addressing recent studies directly comparing different types of motion integration, both in typical and atypical development, and suggest areas ripe for future research.

Long-Lasting Crossmodal Cortical Reorganization Triggered by Brief Postnatal Visual Deprivation.

Animal and human studies have demonstrated that transient visual deprivation early in life, even for a very short period, permanently alters the response properties of neurons in the visual cortex and leads to corresponding behavioral visual deficits. While it is acknowledged that early-onset and longstanding blindness leads the occipital cortex to respond to non-visual stimulation, it remains unknown whether a short and transient period of postnatal visual deprivation is sufficient to trigger crossmodal reorganization that persists after years of visual experience. In the present study, we characterized brain responses to auditory stimuli in 11 adults who had been deprived of all patterned vision at birth by congenital cataracts in both eyes until they were treated at 9 to 238 days of age. When compared to controls with typical visual experience, the cataract-reversal group showed enhanced auditory-driven activity in focal visual regions. A combination of dynamic causal modeling with Bayesian model selection indicated that this auditory-driven activity in the occipital cortex was better explained by direct cortico-cortical connections with the primary auditory cortex than by subcortical connections. Thus, a short and transient period of visual deprivation early in life leads to enduring large-scale crossmodal reorganization of the brain circuitry typically dedicated to vision.

Developmental trends in interpolation and its spatial constraints: A comparison of subjective and occluded contours.

We examined interpolation in 6- and 9-year-old children and in adults, in the two most common forms of fragmentation: subjective and partially occluded contours. Experiment 1 examined the effects on adults' interpolation of contour geometry, specifically, the effect of a scale-dependent factor (i.e., retinal size) and a scale-independent factor (i.e., support ratio). For both subjective and partially occluded contours, interpolation was affected more by support ratio than absolute size. However, subjective contours were less precisely interpolated and their interpolation was affected more by support ratio than was the case for partial occlusion. Experiment 2 used a subset of retinal size and support ratio levels in children and adults. Interpolation of both subjective and occluded contours improved significantly with age, with the two types of contours equally affected by spatial constraints during early childhood. However, while interpolation of occluded contours became more precise with age and less dependent on support ratio by adulthood, interpolation of subjective contours was less improved and became even more tied to support ratio in adulthood. The implications of these differential age-related changes in the spatial constraints on interpolation of the two types of contours for the mechanisms of perceptual completion are discussed.

Developmental mechanisms underlying improved contrast thresholds for discriminations of orientation signals embedded in noise.

We combined an external noise paradigm with an efficient procedure for obtaining contrast thresholds (Lesmes et al., 2006) in order to model developmental changes in the effect of noise on contrast discrimination during childhood. Specifically, we measured the contrast thresholds of 5-, 7-, 9-year-olds and adults (n = 20/age) in a two alternative forced-choice orientation discrimination task over a wide range of external noise levels and at three levels of accuracy. Overall, as age increased, contrast thresholds decreased over the entire range of external noise levels tested. The decrease was greatest between 5 and 7 years of age. The reduction in threshold after age 5 was greater in the high than the low external noise region, a pattern implying greater tolerance of the irrelevant background noise as children became older. To model the mechanisms underlying these developmental changes in terms of internal noise components, we adapted the original perceptual template model (Lu and Dosher, 1998) and normalized the magnitude of performance changes against the performance of 5-year-olds. The resulting model provided an excellent fit (r (2) = 0.985) to the contrast thresholds at multiple levels of accuracy (60, 75, and 90%) across a wide range of external noise levels. The improvements in contrast thresholds with age were best modeled by a combination of reductions in internal additive noise, reductions in internal multiplicative noise, and improvements in excluding external noise by template retuning. In line with the data, the improvement was greatest between 5 and 7 years of age, accompanied by a 39% reduction in additive noise, 71% reduction in multiplicative noise, and 45% improvement in external noise exclusion. The modeled improvements likely reflect developmental changes at the cortical level, rather than changes in front-end structural properties (Kiorpes et al., 2003).

Early visual deprivation from congenital cataracts disrupts activity and functional connectivity in the face network.

The development of the face-processing network has been examined with functional neuroimaging, but the effect of visual deprivation early in life on this network is not known. We examined this question in a group of young adults who had been born with dense, central cataracts in both eyes that blocked all visual input to the retina until the cataracts were removed during infancy. We used functional magnetic resonance imaging to examine regions in the "core" and "extended" face networks as participants viewed faces and other objects, and performed a face discrimination task. This task required matching faces on the basis of facial features or on the spacing between the facial features. The Cataract group (a) had reduced discrimination performance on the Spacing task relative to Controls; (b) used the same brain regions as Controls when passively viewing faces or making judgments about faces, but showed reduced activation during passive viewing of faces, especially in extended face-network regions; and (c) unlike Controls, showed activation in face-network regions for objects. In addition, the functional connections of the fusiform gyri with the rest of the face network were altered, and these brain changes were related to Cataract participants' performance on the face discrimination task. These results provide evidence that early visual input is necessary to set up or preserve activity and functional connectivity in the face-processing network that will later mediate expert face processing.

The effect of early visual deprivation on the development of face detection.

The expertise of adults in face perception is facilitated by their ability to rapidly detect that a stimulus is a face. In two experiments, we examined the role of early visual input in the development of face detection by testing patients who had been treated as infants for bilateral congenital cataract. Experiment 1 indicated that, at age 9 to 20, patients' accuracy and response times on a Mooney face detection task were normal. Experiment 2 revealed that the neural mechanisms underlying face detection in a similar group of adult patients are abnormal: the amplitude of both the P100 and N170 event-related potential were larger in patients than in visually normal controls, and the extent of augmentation was related to the duration of deprivation. Thus, early visual experience is necessary for the establishment of normal neural networks for face detection; abnormalities at these early processing stages may contribute to the deficits we previously reported in configural face processing for this patient cohort.

The effect of video game training on the vision of adults with bilateral deprivation amblyopia.

Amblyopia is a condition involving reduced acuity caused by abnormal visual input during a critical period beginning shortly after birth. Amblyopia is typically considered to be irreversible during adulthood. Here we provide the first demonstration that video game training can improve at least some aspects of the vision of adults with bilateral deprivation amblyopia caused by a history of bilateral congenital cataracts. Specifically, after 40 h of training over one month with an action video game, most patients showed improvement in one or both eyes on a wide variety of tasks including acuity, spatial contrast sensitivity, and sensitivity to global motion. As well, there was evidence of improvement in at least some patients for temporal contrast sensitivity, single letter acuity, crowding, and feature spacing in faces, but not for useful field of view. The results indicate that, long after the end of the critical period for damage, there is enough residual plasticity in the adult visual system to effect improvements, even in cases of deep amblyopia caused by early bilateral deprivation.

Sparing of sensitivity to biological motion but not of global motion after early visual deprivation.

Patients deprived of visual experience during infancy by dense bilateral congenital cataracts later show marked deficits in the perception of global motion (dorsal visual stream) and global form (ventral visual stream). We expected that they would also show marked deficits in sensitivity to biological motion, which is normally processed in the superior temporal sulcus via input from both the dorsal and ventral streams. When tested on the same day for sensitivity to biological motion and to global motion at two speeds (4 and 18° s(-1)), patients, as expected, displayed a large deficit in processing global motion at both speeds. Surprisingly, they performed normally in discriminating biological motion from scrambled displays, tolerating as much noise as their age-matched controls. Networks bypassing damaged portions of the dorsal and the ventral streams must mediate the spared sensitivity to biological motion after early visual deprivation.

Long trajectory for the development of sensitivity to global and biological motion.

We used a staircase procedure to test sensitivity to (1) global motion in random-dot kinematograms moving at 4° and 18° s(-1) and (2) biological motion. Thresholds were defined as (1) the minimum percentage of signal dots (i.e. the maximum percentage of noise dots) necessary for accurate discrimination of upward versus downward motion or (2) the maximum percentage of noise dots tolerated for accurate discrimination of biological from non-biological motion. Subjects were adults and children aged 6-8, 9-11, and 12-14 years (n = 20 per group). Contrary to earlier research, results revealed a similar, long developmental trajectory for sensitivity to global motion at both slower and faster speeds and for biological motion. Thresholds for all three tasks improved monotonically between 6 and 14 years of age, at which point they were adult-like. The results suggest that the extrastriate mechanisms that integrate local motion cues over time and space take many years to mature.

Development of sensitivity to spacing versus feature changes in pictures of houses: Evidence for slow development of a general spacing detection mechanism?

Adults are expert at recognizing faces, in part because of exquisite sensitivity to the spacing of facial features. Children are poorer than adults at recognizing facial identity and less sensitive to spacing differences. Here we examined the specificity of the immaturity by comparing the ability of 8-year-olds, 14-year-olds, and adults to discriminate houses differing in the spacing between features versus those differing in the shape of the features themselves. By 8 years of age, children were more accurate for discriminations involving the feature set compared with the spacing set, and the difference in accuracy compared with adults was greater for the spacing set than for the feature set. Importantly, when sets were matched in difficulty for adults, this greater immaturity on the spacing set than on the feature set remained. The results suggest that, at least by age 8, immaturities in sensitivity to the spacing of features may be related to immaturities in general perceptual mechanisms rather than face-specific mechanisms.