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Neural correlates of natural human echolocation in early and late blind echolocation experts.

Thaler L, Arnott SR, Goodale MA - PLoS ONE (2011)

Bottom Line: When we compared brain activity for sounds that contained both clicks and the returning echoes with brain activity for control sounds that did not contain the echoes, but were otherwise acoustically matched, we found activity in calcarine cortex in both individuals.Importantly, for the same comparison, we did not observe a difference in activity in auditory cortex.These findings suggest that processing of click-echoes recruits brain regions typically devoted to vision rather than audition in both early and late blind echolocation experts.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Western Ontario, London, Ontario, Canada.

ABSTRACT

Background: A small number of blind people are adept at echolocating silent objects simply by producing mouth clicks and listening to the returning echoes. Yet the neural architecture underlying this type of aid-free human echolocation has not been investigated. To tackle this question, we recruited echolocation experts, one early- and one late-blind, and measured functional brain activity in each of them while they listened to their own echolocation sounds.

Results: When we compared brain activity for sounds that contained both clicks and the returning echoes with brain activity for control sounds that did not contain the echoes, but were otherwise acoustically matched, we found activity in calcarine cortex in both individuals. Importantly, for the same comparison, we did not observe a difference in activity in auditory cortex. In the early-blind, but not the late-blind participant, we also found that the calcarine activity was greater for echoes reflected from surfaces located in contralateral space. Finally, in both individuals, we found activation in middle temporal and nearby cortical regions when they listened to echoes reflected from moving targets.

Conclusions: These findings suggest that processing of click-echoes recruits brain regions typically devoted to vision rather than audition in both early and late blind echolocation experts.

Show MeSH
Illustration of click sounds, click echoes and experimental materials, and summary of behavioural results.A: Waveplots and spectrograms of the sound of a click (highlighted with black arrows) and its echo (highlighted with green arrows) recorded in the left (L) and right (R) ears of EB and LB (sampling rate 44.1 kHz) (Sound S1 and Sound S2). Both EB and LB made the clicks in the presence of a position marker (shown in 1B) located straight ahead. Spectrograms were obtained using an FFT window of 256 samples, corresponding to approximately 5.6 ms in our recordings. Waveform plots and spectrograms are for illustration. While the exact properties of the click and its echo (e.g. loudness, timbre) are specific to the person generating the click as well as the sound reflecting surface, prominent characteristics of clicks are short duration (approximately 10 ms) and broad frequency spectra, both of which are evident in the plots. B: Position marker used for angular position discrimination experiments during active echolocation, and to make recordings for the passive listening paradigm. The marker was an aluminium foil covered foam half-tube (diameter 6 cm, height 180 cm), placed vertically, at a distance of 150 cm, with the concave side facing the subject. Note the 125-Hz cutoff wedge system on the walls of the anechoic chamber. C: Results of angular position discrimination experiments (for examples of sound stimuli used during passive listening listen to Sounds S5 and S6). Plotted on the ordinate is the probability that the participant judges the position marker to be located to the right of its straight ahead reference position. Plotted on the abscissa is the position of the test position with respect to the straight ahead in degrees. Negative numbers indicate a position shift in the counter clockwise direction. Psychometric functions were obtained by fitting a 3-parameter sigmoid to the data. 25% and 75% thresholds and bias (denoted in red) were estimated from fitted curves. The zero-bias line (dashed line) is drawn for comparison. D: Stimuli were recorded with microphones placed in the echolocator's ears, directly in front of the ear canal. E: During passive listening, stimuli were delivered using fMRI compatible in-ear headphones, which imposed a 10 kHz cutoff (marked with a dashed line in spectrograms in A). F–G: Behavioral results from the various passive-listening classification tasks (for examples of sound stimuli used during the various classification tasks listen to Sound S7, Sound S8, Sound S9, Sound S10, Sound S11, Sound S12, Sound S13). Shown is percentage correct. Asterisks indicate that performance is significantly different from chance (p<.05). Unless otherwise indicated, chance performance is 50%. Sample sizes (reported in Table S1 and Table S2) fulfil minimum requirement for confidence intervals for a proportion based on the normal approximation [48]. 1 = less than chance, because of bias to classify as ‘tree’.
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pone-0020162-g001: Illustration of click sounds, click echoes and experimental materials, and summary of behavioural results.A: Waveplots and spectrograms of the sound of a click (highlighted with black arrows) and its echo (highlighted with green arrows) recorded in the left (L) and right (R) ears of EB and LB (sampling rate 44.1 kHz) (Sound S1 and Sound S2). Both EB and LB made the clicks in the presence of a position marker (shown in 1B) located straight ahead. Spectrograms were obtained using an FFT window of 256 samples, corresponding to approximately 5.6 ms in our recordings. Waveform plots and spectrograms are for illustration. While the exact properties of the click and its echo (e.g. loudness, timbre) are specific to the person generating the click as well as the sound reflecting surface, prominent characteristics of clicks are short duration (approximately 10 ms) and broad frequency spectra, both of which are evident in the plots. B: Position marker used for angular position discrimination experiments during active echolocation, and to make recordings for the passive listening paradigm. The marker was an aluminium foil covered foam half-tube (diameter 6 cm, height 180 cm), placed vertically, at a distance of 150 cm, with the concave side facing the subject. Note the 125-Hz cutoff wedge system on the walls of the anechoic chamber. C: Results of angular position discrimination experiments (for examples of sound stimuli used during passive listening listen to Sounds S5 and S6). Plotted on the ordinate is the probability that the participant judges the position marker to be located to the right of its straight ahead reference position. Plotted on the abscissa is the position of the test position with respect to the straight ahead in degrees. Negative numbers indicate a position shift in the counter clockwise direction. Psychometric functions were obtained by fitting a 3-parameter sigmoid to the data. 25% and 75% thresholds and bias (denoted in red) were estimated from fitted curves. The zero-bias line (dashed line) is drawn for comparison. D: Stimuli were recorded with microphones placed in the echolocator's ears, directly in front of the ear canal. E: During passive listening, stimuli were delivered using fMRI compatible in-ear headphones, which imposed a 10 kHz cutoff (marked with a dashed line in spectrograms in A). F–G: Behavioral results from the various passive-listening classification tasks (for examples of sound stimuli used during the various classification tasks listen to Sound S7, Sound S8, Sound S9, Sound S10, Sound S11, Sound S12, Sound S13). Shown is percentage correct. Asterisks indicate that performance is significantly different from chance (p<.05). Unless otherwise indicated, chance performance is 50%. Sample sizes (reported in Table S1 and Table S2) fulfil minimum requirement for confidence intervals for a proportion based on the normal approximation [48]. 1 = less than chance, because of bias to classify as ‘tree’.

Mentions: Research has shown that people, like many animals, are capable of using reflected sound waves (i.e. echoes) to perceive attributes of their silent physical environment (for reviews see [1]–[3]). Although this ability can been promoted through technological aids (e.g. [4]–[7]), such devices are by no means a necessary requirement. Indeed, there is increasing recognition of the fact that some people can actively echolocate without the use of any peripheral aids whatsoever [3]. The enormous potential of this ‘natural’ echolocation ability is realized in a segment of the blind population that has learned to sense silent objects in the environment simply by generating clicks with their tongues and mouths and then listening to the returning echoes [8]. The echolocation click produced by such individuals tends to be short (approximately 10 ms) and spectrally broad (Figure 1A; Sound S1 and Sound S2). Clicks can be produced in various ways, but it has been suggested that the palatal click, produced by quickly moving the tongue backwards and downwards from the palatal region directly behind the teeth, is best for natural human echolocation [9]. For the skilled echolocator, the returning echoes can potentially provide a great deal of information regarding the position, distance, size, shape and texture of objects [3].


Neural correlates of natural human echolocation in early and late blind echolocation experts.

Thaler L, Arnott SR, Goodale MA - PLoS ONE (2011)

Illustration of click sounds, click echoes and experimental materials, and summary of behavioural results.A: Waveplots and spectrograms of the sound of a click (highlighted with black arrows) and its echo (highlighted with green arrows) recorded in the left (L) and right (R) ears of EB and LB (sampling rate 44.1 kHz) (Sound S1 and Sound S2). Both EB and LB made the clicks in the presence of a position marker (shown in 1B) located straight ahead. Spectrograms were obtained using an FFT window of 256 samples, corresponding to approximately 5.6 ms in our recordings. Waveform plots and spectrograms are for illustration. While the exact properties of the click and its echo (e.g. loudness, timbre) are specific to the person generating the click as well as the sound reflecting surface, prominent characteristics of clicks are short duration (approximately 10 ms) and broad frequency spectra, both of which are evident in the plots. B: Position marker used for angular position discrimination experiments during active echolocation, and to make recordings for the passive listening paradigm. The marker was an aluminium foil covered foam half-tube (diameter 6 cm, height 180 cm), placed vertically, at a distance of 150 cm, with the concave side facing the subject. Note the 125-Hz cutoff wedge system on the walls of the anechoic chamber. C: Results of angular position discrimination experiments (for examples of sound stimuli used during passive listening listen to Sounds S5 and S6). Plotted on the ordinate is the probability that the participant judges the position marker to be located to the right of its straight ahead reference position. Plotted on the abscissa is the position of the test position with respect to the straight ahead in degrees. Negative numbers indicate a position shift in the counter clockwise direction. Psychometric functions were obtained by fitting a 3-parameter sigmoid to the data. 25% and 75% thresholds and bias (denoted in red) were estimated from fitted curves. The zero-bias line (dashed line) is drawn for comparison. D: Stimuli were recorded with microphones placed in the echolocator's ears, directly in front of the ear canal. E: During passive listening, stimuli were delivered using fMRI compatible in-ear headphones, which imposed a 10 kHz cutoff (marked with a dashed line in spectrograms in A). F–G: Behavioral results from the various passive-listening classification tasks (for examples of sound stimuli used during the various classification tasks listen to Sound S7, Sound S8, Sound S9, Sound S10, Sound S11, Sound S12, Sound S13). Shown is percentage correct. Asterisks indicate that performance is significantly different from chance (p<.05). Unless otherwise indicated, chance performance is 50%. Sample sizes (reported in Table S1 and Table S2) fulfil minimum requirement for confidence intervals for a proportion based on the normal approximation [48]. 1 = less than chance, because of bias to classify as ‘tree’.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3102086&req=5

pone-0020162-g001: Illustration of click sounds, click echoes and experimental materials, and summary of behavioural results.A: Waveplots and spectrograms of the sound of a click (highlighted with black arrows) and its echo (highlighted with green arrows) recorded in the left (L) and right (R) ears of EB and LB (sampling rate 44.1 kHz) (Sound S1 and Sound S2). Both EB and LB made the clicks in the presence of a position marker (shown in 1B) located straight ahead. Spectrograms were obtained using an FFT window of 256 samples, corresponding to approximately 5.6 ms in our recordings. Waveform plots and spectrograms are for illustration. While the exact properties of the click and its echo (e.g. loudness, timbre) are specific to the person generating the click as well as the sound reflecting surface, prominent characteristics of clicks are short duration (approximately 10 ms) and broad frequency spectra, both of which are evident in the plots. B: Position marker used for angular position discrimination experiments during active echolocation, and to make recordings for the passive listening paradigm. The marker was an aluminium foil covered foam half-tube (diameter 6 cm, height 180 cm), placed vertically, at a distance of 150 cm, with the concave side facing the subject. Note the 125-Hz cutoff wedge system on the walls of the anechoic chamber. C: Results of angular position discrimination experiments (for examples of sound stimuli used during passive listening listen to Sounds S5 and S6). Plotted on the ordinate is the probability that the participant judges the position marker to be located to the right of its straight ahead reference position. Plotted on the abscissa is the position of the test position with respect to the straight ahead in degrees. Negative numbers indicate a position shift in the counter clockwise direction. Psychometric functions were obtained by fitting a 3-parameter sigmoid to the data. 25% and 75% thresholds and bias (denoted in red) were estimated from fitted curves. The zero-bias line (dashed line) is drawn for comparison. D: Stimuli were recorded with microphones placed in the echolocator's ears, directly in front of the ear canal. E: During passive listening, stimuli were delivered using fMRI compatible in-ear headphones, which imposed a 10 kHz cutoff (marked with a dashed line in spectrograms in A). F–G: Behavioral results from the various passive-listening classification tasks (for examples of sound stimuli used during the various classification tasks listen to Sound S7, Sound S8, Sound S9, Sound S10, Sound S11, Sound S12, Sound S13). Shown is percentage correct. Asterisks indicate that performance is significantly different from chance (p<.05). Unless otherwise indicated, chance performance is 50%. Sample sizes (reported in Table S1 and Table S2) fulfil minimum requirement for confidence intervals for a proportion based on the normal approximation [48]. 1 = less than chance, because of bias to classify as ‘tree’.
Mentions: Research has shown that people, like many animals, are capable of using reflected sound waves (i.e. echoes) to perceive attributes of their silent physical environment (for reviews see [1]–[3]). Although this ability can been promoted through technological aids (e.g. [4]–[7]), such devices are by no means a necessary requirement. Indeed, there is increasing recognition of the fact that some people can actively echolocate without the use of any peripheral aids whatsoever [3]. The enormous potential of this ‘natural’ echolocation ability is realized in a segment of the blind population that has learned to sense silent objects in the environment simply by generating clicks with their tongues and mouths and then listening to the returning echoes [8]. The echolocation click produced by such individuals tends to be short (approximately 10 ms) and spectrally broad (Figure 1A; Sound S1 and Sound S2). Clicks can be produced in various ways, but it has been suggested that the palatal click, produced by quickly moving the tongue backwards and downwards from the palatal region directly behind the teeth, is best for natural human echolocation [9]. For the skilled echolocator, the returning echoes can potentially provide a great deal of information regarding the position, distance, size, shape and texture of objects [3].

Bottom Line: When we compared brain activity for sounds that contained both clicks and the returning echoes with brain activity for control sounds that did not contain the echoes, but were otherwise acoustically matched, we found activity in calcarine cortex in both individuals.Importantly, for the same comparison, we did not observe a difference in activity in auditory cortex.These findings suggest that processing of click-echoes recruits brain regions typically devoted to vision rather than audition in both early and late blind echolocation experts.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Western Ontario, London, Ontario, Canada.

ABSTRACT

Background: A small number of blind people are adept at echolocating silent objects simply by producing mouth clicks and listening to the returning echoes. Yet the neural architecture underlying this type of aid-free human echolocation has not been investigated. To tackle this question, we recruited echolocation experts, one early- and one late-blind, and measured functional brain activity in each of them while they listened to their own echolocation sounds.

Results: When we compared brain activity for sounds that contained both clicks and the returning echoes with brain activity for control sounds that did not contain the echoes, but were otherwise acoustically matched, we found activity in calcarine cortex in both individuals. Importantly, for the same comparison, we did not observe a difference in activity in auditory cortex. In the early-blind, but not the late-blind participant, we also found that the calcarine activity was greater for echoes reflected from surfaces located in contralateral space. Finally, in both individuals, we found activation in middle temporal and nearby cortical regions when they listened to echoes reflected from moving targets.

Conclusions: These findings suggest that processing of click-echoes recruits brain regions typically devoted to vision rather than audition in both early and late blind echolocation experts.

Show MeSH