Stefania S. Moro

No Colavita effect: equal auditory and visual processing in people with one eye

Previous research has shown that people with one eye have enhanced spatial vision implying intra-modal compensation for their loss of binocularity. The current experiments investigate whether monocular blindness from unilateral eye enucleation may lead to cross-modal sensory compensation for the loss of one eye. We measured speeded detection and discrimination of audiovisual targets presented as a stream of paired objects and familiar sounds in a group of individuals with monocular enucleation compared to controls viewing binocularly or monocularly. In Experiment 1, participants detected the presence of auditory, visual or audiovisual targets. All participant groups were equally able to detect the targets. In Experiment 2, participants discriminated between the visual, auditory or bimodal (audiovisual) targets. Both control groups showed the Colavita effect, that is, preferential processing of visual over auditory information for the bimodal stimuli. The monocular enucleation group, however, showed no Colavita effect, and further, they demonstrated equal processing of visual and auditory stimuli. This finding suggests a lack of visual dominance and equivalent auditory and visual processing in people with one eye. This may be an adaptive form of sensory compensation for the loss of one eye and could result from recruitment of deafferented visual cortical areas by inputs from other senses.

Optimal Audiovisual Integration in People with One Eye

People with one eye show altered sensory processing. Such changes might reflect a central reweighting of sensory information that might impact on how multisensory cues are integrated. We assessed whether people who lost an eye early in life differ from controls with respect to audiovisual integration. In order to quantify the relative weightings assigned to each sensory system, participants were asked to spatially localize audiovisual events that have been previously shown to be optimally combined and perceptually fused from the point of view of location in a normal population, where the auditory and visual components were spatially disparate. There was no difference in the variability of localizing unimodal visual and auditory targets by people with one eye compared to controls. People with one eye did however, demonstrate slower reaction times to localize visual stimuli compared to auditory stimuli and were slower than binocular and eye-patched control groups. When localizing bimodal targets, the weightings assigned to each sensory modality in both people with one eye and controls were predictable from their unimodal performance, in accordance with Maximum Likelihood Estimation and the time it took all three groups to localize the bimodal targets was faster than for vision alone. Regardless of demonstrating a longer response time to visual stimuli, people with one eye appear to integrate the auditory and visual components of multisensory events optimally when determining spatial location.

No Colavita effect: increasing temporal load maintains equal auditory and visual processing in people with one eye.

We investigate whether the loss of one eye leads to enhanced multisensory processing. Previously, we measured discrimination of auditory, visual and audiovisual targets in people with one eye compared to controls viewing binocularly or with one eye patched. Both control groups demonstrated typical visual dominance (the Colavita effect) whereas people with one eye show no Colavita effect, and instead show equal preference for visual and auditory stimuli. Here, we loaded temporal processing in an attempt to favour audition and thereby reverse Colavita visual dominance with a modified repetition blindness paradigm. The Colavita effect was reduced for controls however, people with one eye continued to show no Colavita effect, reversed or otherwise. People with one eye display equal auditory and visual processing in this context, suggesting unbiased multisensory processing, likely as a form of cross-modal adaptation and compensation for their loss of binocularity.

Audiovisual integration in people with one eye: Normal temporal binding window and sound induced flash illusion but reduced McGurk effect

INTRODUCTION Previously, we have shown that people with one eye have enhanced sound localization (Hoover, Harris & Steeves, 2012, EBR) and lack the visual dominance commonly found in binocular and patched viewing controls (Moro & Steeves, 2011, EBR). These results persist despite evidence that their integration of the auditory and visual components of multisensory events, when determining spatial location, is optimal (Moro, Harris & Steeves, 2014, MSR). Currently, we conducted three behavioural studies to further explore audiovisual integration in people with one eye compared to binocular and patched viewing controls. Experiment 1. We investigated the temporal component of audiovisual integration, by measuring the temporal binding window (TBW). Participants performed an audiovisual simultaneity judgment task and people with one eye showed no difference in width of TBW compared to controls despite slower performance. Experiment 2. We measured the sound induced flash illusion (SF) where participants indicated the number of light flashes paired with multiple tones. People with one eye performed no differently from controls. Experiment 3. We measured the McGurk audiovisual illusion. People with one eye showed a reduced McGurk effect compared to controls. CONCLUSIONS It is possible that these mixed findings reflect differences in levels of processing between the three tasks. Higher level audiovisual processing (McGurk) compared to lower level audiovisual processing (TBW and SF) might benefit more from potential changes in underlying neural connectivity with eye enucleation early in life. These findings provide further evidence for changes in sensory neural connectivity in people with one eye that may serve as cross-modal adaptation for the loss of binocularity during early brain development. Meeting abstract presented at VSS 2015.

Altered white matter structure in the visual system following early monocular enucleation

Partial visual deprivation from early monocular enucleation (the surgical removal of one eye within the first few years of life) results in a number of long‐term morphological adaptations in adult cortical and subcortical visual, auditory, and multisensory brain regions. In this study, we investigated whether early monocular enucleation also results in the altered development of white matter structure. Diffusion tensor imaging and probabilistic tractography were performed to assess potential differences in visual system white matter in adult participants who had undergone early monocular enucleation compared to binocularly intact controls. To examine the microstructural properties of these tracts, mean diffusion parameters including fractional anisotropy (FA), mean diffusivity (MD), axial diffusivity (AD), and radial diffusivity (RD) were extracted bilaterally. Asymmetries opposite to those observed in controls were found for FA, MD, and RD in the optic radiations, the projections from primary visual cortex (V1) to the lateral geniculate nucleus (LGN), and the interhemispheric V1 projections of early monocular enucleation participants. Early monocular enucleation was also associated with significantly lower FA bidirectionally in the interhemispheric V1 projections. These differences were consistently greater for the tracts contralateral to the enucleated eye, and are consistent with the asymmetric LGN volumes and optic tract diameters previously demonstrated in this group of participants. Overall, these results indicate that early monocular enucleation has long‐term effects on white matter structure in the visual pathway that results in reduced fiber organization in tracts contralateral to the enucleated eye. Hum Brain Mapp 39:133–144, 2018.

Evidence of multisensory plasticity: Asymmetrical medial geniculate body in people with one eye.

The medial geniculate body (MGB) plays a central role in auditory processing with both efferent and afferent tracts to primary auditory cortex. People who have lost one eye early in life have enhanced sound localization, lack visual over auditory dominance and integrate auditory and visual information optimally, similar to controls, despite taking longer to localize unimodal visual stimuli. Compared to controls, people with one eye have decreased lateral geniculate nuclei (LGN) volume as expected given the 50% deafferentation of the visual system. However, LGN volume is larger than predicted contralateral to the remaining eye, indicating altered structural development likely through recruitment of deafferented LGN cells. Purpose: the current study investigated whether structural MGB changes are also present in this group given the changes they exhibit in auditory processing. Methods: MGB volumes were measured in adults who had undergone early unilateral eye enucleation and were compared to binocularly intact controls. Results: unlike controls, people with one eye had a significant asymmetry with a larger left compared to right MGB, independent of eye of enucleation. MGB volume correlated positively with LGN volume in people with one eye. Conclusions: volume asymmetry in the MGB in people with one eye may represent increased interactions between the left MGB and primary auditory cortex. This interaction could contribute to increased auditory and other left hemisphere-dominant processing, including language, as compensation for the loss of one half of visual inputs early in life. The positive correlation between MGB and LGN volume is not due to space constraints but rather indicates increased plasticity in both auditory and visual sensory systems following early eye enucleation.

Normal temporal binding window but no sound-induced flash illusion in people with one eye

Integrating vision and hearing is an important way in which we process our rich sensory environment. Partial deprivation of the visual system from the loss of one eye early in life results in adaptive changes in the remaining senses (e.g., Hoover et al. in Exp Brain Res 216:565–74, 2012). The current study investigates whether losing one eye early in life impacts the temporal window in which audiovisual events are integrated and whether there is vulnerability to the sound-induced flash illusion. In Experiment 1, we measured the temporal binding window with a simultaneity judgement task where low-level auditory and visual stimuli were presented at different stimulus onset asynchronies. People with one eye did not differ in the width of their temporal binding window, but they took longer to make judgements compared to binocular viewing controls. In Experiment 2, we measured how many light flashes were perceived when a single flash was paired with multiple auditory beeps in close succession (sound induced flash illusion). Unlike controls, who perceived multiple light flashes with two, three or four beeps, people with one eye were not susceptible to the sound-induced flash illusion. In addition, they took no longer to respond compared to both binocular and monocular (eye-patched) viewing controls. Taken together, these results suggest that the lack of susceptibility to the sound-induced flash illusion in people with one eye cannot be accounted for by the width of the temporal binding window. These results provide evidence for adaptations in audiovisual integration due to the reduction of visual input from the loss of one eye early in life.

Short and long-term visual deprivation leads to adapted use of audiovisual information for face-voice recognition

Person identification is essential for everyday social interactions. We quickly identify people from cues such as a persons face or the sound of their voice. A change in sensory input, such as losing ones vision, can alter how one uses sensory information. We asked how people with only one eye, who have had reduced visual input during postnatal maturation of the visual system, use faces and voices for person identity recognition. We used an old/new paradigm to investigate unimodal (visual or auditory) and bimodal (audiovisual) identity recognition of people (face, voice and face-voice) and a control category, objects (car, horn and car-horn). Participants learned the identity of 10 pairs of faces and voices (Experiment 1) and 10 cars and horns (Experiment 2) and were asked to identify the learned face/voice or car/horn among 20 distractors. People with one eye were more sensitive to voice identification compared to controls viewing binocularly or with an eye-patch. However, both people with one eye and eye-patched viewing controls use combined audiovisual information for person identification more equally than binocular viewing controls, who favour vision. People with one eye were no different from controls at object identification. The observed visual dominance for binocular controls is larger for person compared to object identification, indicating that faces (vision) play a larger role in person identification and that person identity processing is unique from that for objects. People with long-term visual deprivation from the loss of one eye may have adaptive strategies, such as placing less reliance on vision to achieve intact performance, particularly for face processing.

Audiovisual plasticity following early abnormal visual experience: Reduced McGurk effect in people with one eye

Previously, we have shown that people who have had one eye surgically removed early in life during visual development have enhanced sound localization [1] and lack visual dominance, commonly observed in binocular and monocular (eye-patched) viewing controls [2]. Despite these changes, people with one eye integrate auditory and visual components of multisensory events optimally [3]. The current study investigates how people with one eye perceive the McGurk effect, an audiovisual illusion where a new syllable is perceived when visual lip movements do not match the corresponding sound [4]. We compared individuals with one eye to binocular and monocular viewing controls and found that they have a significantly smaller McGurk effect compared to binocular controls. Additionally, monocular controls tended to perceive the McGurk effect less often than binocular controls suggesting a small transient modulation of the McGurk effect. These results suggest altered weighting of the auditory and visual modalities with both short and long-term monocular viewing. These results indicate the presence of permanent adaptive perceptual accommodations in people who have lost one eye early in life that may serve to mitigate the loss of binocularity during early brain development.

Intact Dynamic Visual Capture in People With One Eye

Observing motion in one modality can influence the perceived direction of motion in a second modality (dynamic capture). For example observing a square moving in depth can influence the perception of a sound to increase in loudness. The current study investigates whether people who have lost one eye are susceptible to audiovisual dynamic capture in the depth plane similar to binocular and eye-patched viewing control participants. Partial deprivation of the visual system from the loss of one eye early in life results in changes in the remaining intact senses such as hearing. Linearly expanding or contracting discs were paired with increasing or decreasing tones and participants were asked to indicate the direction of the auditory stimulus. Magnitude of dynamic visual capture was measured in people with one eye compared to eye-patched and binocular viewing controls. People with one eye have the same susceptibility to dynamic visual capture as controls, where they perceived the direction of the auditory signal to be moving in the direction of the incongruent visual signal, despite previously showing a lack of visual dominance for audiovisual cues. This behaviour may be the result of directing attention to the visual modality, their partially deficient sense, in order to gain important information about approaching and receding stimuli which in the former case could be life-threatening. These results contribute to the growing body of research showing that people with one eye display unique accommodations with respect to audiovisual processing that are likely adaptive in each unique sensory situation.