Neural correlates of motion processing through echolocation, source hearing, and vision in blind echolocation experts and sighted echolocation novices

Abstract

Thaler L, Milne JL, Arnott SR, Kish D, Goodale MA. Neural correlates of motion processing through echolocation, source hearing, and vision in blind echolocation experts and sighted echolocation novices. J Neurophysiol 111: 112-127, 2014. First published October 16, 2013 doi:10.1152/jn.00501.2013.-We have shown in previous research (Thaler L, Arnott SR, Goodale MA. PLoS One 6: e20162, 2011) that motion processing through echolocation activates temporal-occipital cortex in blind echolocation experts. Here we investigated how neural substrates of echo-motion are related to neural substrates of auditory source-motion and visual-motion. Three blind echolocation experts and twelve sighted echolocation novices underwent functional MRI scanning while they listened to binaural recordings of moving or stationary echolocation or auditory source sounds located either in left or right space. Sighted participants' brain activity was also measured while they viewed moving or stationary visual stimuli. For each of the three modalities separately (echo, source, vision), we then identified motion-sensitive areas in temporal-occipital cortex and in the planum temporale. We then used a region of interest (ROI) analysis to investigate cross-modal responses, as well as laterality effects. In both sighted novices and blind experts, we found that temporal-occipital source-motion ROIs did not respond to echo-motion, and echo-motion ROIs did not respond to sourcemotion. This double-dissociation was absent in planum temporale ROIs. Furthermore, temporal-occipital echo-motion ROIs in blind, but not sighted, participants showed evidence for contralateral motion preference. Temporal-occipital source-motion ROIs did not show evidence for contralateral preference in either blind or sighted participants. Our data suggest a functional segregation of processing of auditory source-motion and echo-motion in human temporal-occipital cortex. Furthermore, the data suggest that the echo-motion response in blind experts may represent a reorganization rather than exaggeration of response observed in sighted novices. There is the possibility that this reorganization involves the recruitment of "visual" cortical areas.fMRI; human; cortex; neuroplasticity; audition SOME PEOPLE, JUST LIKE CERTAIN bats and marine mammals, can echolocate by making mouth-clicks and listening to the returning echoes (Schenkman and Nilsson 2010;Stoffregen and Pittenger 1995;Teng and Whitney 2011). Echolocation can be learned by both blind and sighted people with normal hearing (Ammons et al. 1953;Teng and Whitney 2011;Worchel and Mauney 1951). Previous behavioral research has shown that people are sensitive to echo-motion (Rosenblum et al. 2000;Thaler et al. 2011), and in a previous functional magnetic resonance imaging (fMRI) study, we found that echoes from moving compared with stationary surfaces elicited an increase in activation in temporal-occipital cortex in blind echolocation experts (Thaler et al. 2011). Human temporal-occipital cortex harbors visual-motion area MTϩ, as...

Human Exploration of Enclosed Spaces through Echolocation

“…Recruiting was an issue because of the time investment in training sighted subjects. Our results are also supported by previous work on the relationship between acoustic features of echolocation vocalizations and performance for object detection (Thaler and Castillo-Serrano, 2016).…”

“…Neuroimaging studies on echolocation have shown that the presentation of spatialized echoes to blind echolocation experts results in strong activations of visual cortical areas (Thaler et al, 2011(Thaler et al, , 2014b. In these studies, participants did not vocalize during imaging, an approach we will refer to as "passive echolocation."…”

“…The binaural room impulse response (BRIR), a measure from architectural acoustics of the reverberant properties of enclosed spaces (Blauert and Lindemann, 1986;Hidaka and Beranek, 2000), captures the complete spatial and temporal distribution of reflections that a sound undergoes from a specific source to a binaural receiver. In a recent study, we introduced a technique allowing subjects to actively produce tongue clicks in the MRI and evaluate real-time generated echoes from a virtual reflector (Wallmeier et al, 2015). Here, we used this same technique but with a virtual echo-acoustic space, defined by its BRIR, to examine the brain regions recruited during human echolocation.…”

Correlation between vividness of visual imagery and echolocation ability in sighted, echo-naïve people

“…Thus, we would expect this relationship between VVI and echo ability to generalize to other echolocation tasks, unless performance in the echolocation task did not involve calcarine cortex. In recent work we have shown that processing of echo-motion in blind and sighted people relies on activity in temporal-occipital, rather than calcarine cortex (Thaler et al 2013a). Based on this we would expect that performance in an echolocation task that relies exclusively on processing of echo-motion should not correlate with VVI.…”

“…Ammons et al 1953;Worchel and Mauney 1951) and that reflected sound waves can provide skilled echolocators with a wealth of useful information about the reflecting object -e.g. position, distance, size, and density (for reviews see for example Schenkman and Nilsson 2010;Stoffregen and Pittenger 1995), as well as motion (Rosenblum et al 2000;Thaler et al 2013a). On a purely physical basis, information about these properties is carried through mono-and binaural variations in echo timing, spectrum (pitch) and intensity (loudness), and people may be able to exploit these variables for echolocation (Cotzin and Dallenbach 1950;Papadopoulos et al 2011;Rosenblum et al 2000;Schenkman and Nilsson 2010;Stoffregen and Pittenger 1995), though the use of one or the other acoustic variable may also depend on the echolocation task people engage in.…”