In this study we report for the first time gross deficits in auditory spatial localization along the horizontal axis in the congenitally blind: for three of our subjects, thresholds for auditory localization were 3–5-fold worse than those of typical controls, and five of them could not do the task at all. This deficit is far larger than the perceptual enhancements that have been reported, and was evident only for the bisection task: minimal audible angle thresholds were well within the typical range, as were thresholds for simple pointing. What is special about bisection? A decision in a bisection task is not based on an instantaneous estimate but requires a representation of space that must remain in memory for the duration of the task (1 s), and therefore taxes heavily a topographical spatial map. One possibility is that the succession of sounds is interpreted differently by the blind, possibly more as apparent motion, and this interferes with the spatial representation. Blind subjects indeed seem to have lower auditory-motion thresholds than sighted subjects (Lewald, 2013
). However, the fact that their thresholds were not improved by slowing the stimulus presentation to 1-s stimulus separation speaks against this suggestion.
We have previously used this identical task to measure thresholds in children as young as 6 years of age: they had no difficulty in understanding the task, and their thresholds were close to those of adults (Gori et al., 2012a
). By 10 years of age, thresholds had reached adult levels (). Note also that the blind subjects had no difficulty with the temporal bisection, showing that the concept of bisection was not alien to them.
The spatial auditory deficit was specific for the spatial bisection task, which requires subjects to encode the position of three sounds, remember them over a period of 1 s and compare their remembered positions. That there was no deficit for the temporal bisection suggests that there was no deficit in memory per se. Nor was there a deficit in pointing to single targets. It seems that the subjects had a preserved topological representation of space, but an impaired Euclidian representation. Our paradigm did not involve jittering the positions of the two end speakers, so in principle, subjects could have performed the task by ignoring those and attending only to the central speaker. However, the poor thresholds for the blind suggest that they did not (or could not) use this strategy. With a limited group of sighted subjects, we measured bisection thresholds with the end positions jittered and found that it did not affect their results.
Although reduced auditory resolution may seem inconsistent with evidence of enhanced auditory performance and auditory colonization of visual cortex in the blind, it is consistent with the effects of visual deprivation on development of spatial maps in the superior colliculus of guinea pigs, ferrets and cats (Withington-Wray et al., 1990
; King and Carlile, 1993
; Wallace and Stein, 2007
): the maps do develop, but are less well-ordered than in animals reared under normal lighting conditions. We do not know if the spatial bisection task in humans relies on the superior colliculus, rather than a cortical map; but if so, the effects of deprivation on development of the maps would be consistent with preserved topography, but impaired Euclidian representation.
There is good evidence that the visual system is fundamental in calibrating auditory localization: owls reared with distorting prisms show systematic and persistent biases in auditory localization (Knudsen and Knudsen, 1985
); early visual deprivation of ferrets causes disordered development of superior collicular auditory spatial maps (King and Carlile, 1993
); altered vision modifies the developing auditory map (King et al., 1988
; Knudsen and Brainard, 1991
; DeBello et al., 2001
); and relatively brief periods of adaptation to spatially conflicting visual and auditory stimuli biases auditory localization in adults (Recanzone, 1998
; Zwiers et al., 2003
). Interestingly, in children <12 years of age, vision dominates over audition in spatial localization tasks along the horizontal axis, rather than integrating optimally, as in adults (Gori et al., 2012a
), implying that in the developing child, calibration of the auditory system by the visual one is fundamental. These results point to the importance of vision in the formation of auditory spatial maps.
In previous studies we have highlighted the role of cross-sensory calibration in the developing child (Gori et al., 2008
; Burr et al., 2011
; Burr and Gori, 2011
). We believe this to be a general property of sensory systems, particularly during development, when the sensory apparatus is still maturing. The idea, which goes back to Berkley’s (1709/1963)
proposition that touch calibrates vision, is that the more ‘robust and accurate’ sense for a particular sensory task (not necessarily more precise) calibrates the other: a deficit in the more accurate ‘calibrating’ sense should also impact on the system it should calibrate. Following this prediction we have shown that congenitally blind subjects show severe but selective impairments in haptic discrimination tasks, for orientation but not size discriminations (Gori et al., 2010
); and conversely, haptically impaired patients show poor visual size discrimination but not orientation discrimination (Gori et al., 2012b
). The direction of the effects are consistent with the fact that in children <8 years of age, touch dominates vision in size judgements, and vision dominates touch in orientation judgements (Gori et al., 2008
). Interestingly, in both cases the results were quite different with patients with acquired rather than congenital disabilities, suggesting that cross-sensory calibration at an early age is essential.
The present study provides strong evidence for cross-sensory calibration (Burr and Gori, 2011
), suggesting that visual information is necessary for normal development of the auditory sense of space. Blind subjects were not uniformly bad at auditory tasks, but only in the particular bisection task, designed to tax a sophisticated, and well-calibrated spatial auditory map of Euclidean relationships. The simpler tasks tapping minimal audible angle and simple topographical representations may be achieved by less subtle mechanisms.
Besides the obvious theoretical relevance of the study, demonstrating impaired auditory localization and pointing to the role of cross-sensory interactions for normal development, the study could have repercussions for rehabilitation. Blind people rely strongly on auditory information to orient them in the environment. Sturdy spatial maps are clearly of paramount importance and their development in the absence of visual information has to be understood and recovered if impaired. It is possible that techniques could be devised where other senses, such as touch, can serve to calibrate the auditory spatial sense during development.