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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
BOLD activity projected on participants reconstructed and partially inflated cortical surface.Concavities and convexities are colored dark and light, respectively. CS-central sulcus, CaS-calcarine sulcus, LS- lateral sulcus, MFS – middle frontal sulcus. Top panel: BOLD activity while EB and LB listened to recordings of their own echolocation sounds that had been made in an anechoic chamber and judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Bottom Panel: BOLD activity while C1 and C2 listened to recordings they had trained with, i.e. EB and LB's echolocation sounds, respectively. Just as EB and LB, C1 and C2 judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Both EB and LB, but not C1 or C2, show reliable BOLD activity in calcarine sulcus, typically associated with the processing of visual stimuli. EB shows more BOLD activity in calcarine sulcus than LB. All subjects (except C2) also show BOLD activity along the central sulcus (i.e. Motor Cortex) of the left hemisphere, most likely due to the response related right-hand button press. All subjects also show BOLD activity in the lateral sulcus (i.e. Auditory Complex) of the left and right hemispheres and adjacent and inferior to the right medial frontal sulcus. The former likely reflects the auditory nature of the stimuli. The latter most likely reflects the involvement of higher order cognitive and executive control processes during task performance.
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pone-0020162-g002: BOLD activity projected on participants reconstructed and partially inflated cortical surface.Concavities and convexities are colored dark and light, respectively. CS-central sulcus, CaS-calcarine sulcus, LS- lateral sulcus, MFS – middle frontal sulcus. Top panel: BOLD activity while EB and LB listened to recordings of their own echolocation sounds that had been made in an anechoic chamber and judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Bottom Panel: BOLD activity while C1 and C2 listened to recordings they had trained with, i.e. EB and LB's echolocation sounds, respectively. Just as EB and LB, C1 and C2 judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Both EB and LB, but not C1 or C2, show reliable BOLD activity in calcarine sulcus, typically associated with the processing of visual stimuli. EB shows more BOLD activity in calcarine sulcus than LB. All subjects (except C2) also show BOLD activity along the central sulcus (i.e. Motor Cortex) of the left hemisphere, most likely due to the response related right-hand button press. All subjects also show BOLD activity in the lateral sulcus (i.e. Auditory Complex) of the left and right hemispheres and adjacent and inferior to the right medial frontal sulcus. The former likely reflects the auditory nature of the stimuli. The latter most likely reflects the involvement of higher order cognitive and executive control processes during task performance.

Mentions: Functional MRI revealed reliable blood-oxygen-level dependent (BOLD) activity in auditory cortex as well as in the calcarine sulcus and surrounding regions of “visual” cortex in EB and LB when they listened to recordings of their echolocation clicks and echoes, as compared to silence (Figure 2, top). EB showed stronger activity in the calcarine cortex than did LB, which could reflect EB's much longer use of echolocation and/or his more reliable performance in passive echolocation tasks. Activity in calcarine cortex was entirely absent in C1 and C2 when they listened to the echolocation recordings of EB and LB, although both control subjects showed robust activity in auditory cortex (Figure 2, bottom). This pattern of results was expected based on previous experiments that have measured brain activation in blind and sighted people in response to auditory stimulation as compared to silence [13]–[15].


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

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

BOLD activity projected on participants reconstructed and partially inflated cortical surface.Concavities and convexities are colored dark and light, respectively. CS-central sulcus, CaS-calcarine sulcus, LS- lateral sulcus, MFS – middle frontal sulcus. Top panel: BOLD activity while EB and LB listened to recordings of their own echolocation sounds that had been made in an anechoic chamber and judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Bottom Panel: BOLD activity while C1 and C2 listened to recordings they had trained with, i.e. EB and LB's echolocation sounds, respectively. Just as EB and LB, C1 and C2 judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Both EB and LB, but not C1 or C2, show reliable BOLD activity in calcarine sulcus, typically associated with the processing of visual stimuli. EB shows more BOLD activity in calcarine sulcus than LB. All subjects (except C2) also show BOLD activity along the central sulcus (i.e. Motor Cortex) of the left hemisphere, most likely due to the response related right-hand button press. All subjects also show BOLD activity in the lateral sulcus (i.e. Auditory Complex) of the left and right hemispheres and adjacent and inferior to the right medial frontal sulcus. The former likely reflects the auditory nature of the stimuli. The latter most likely reflects the involvement of higher order cognitive and executive control processes during task performance.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0020162-g002: BOLD activity projected on participants reconstructed and partially inflated cortical surface.Concavities and convexities are colored dark and light, respectively. CS-central sulcus, CaS-calcarine sulcus, LS- lateral sulcus, MFS – middle frontal sulcus. Top panel: BOLD activity while EB and LB listened to recordings of their own echolocation sounds that had been made in an anechoic chamber and judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Bottom Panel: BOLD activity while C1 and C2 listened to recordings they had trained with, i.e. EB and LB's echolocation sounds, respectively. Just as EB and LB, C1 and C2 judged the location (left vs. right), shape (concave vs. flat) or stability (moving vs. stationary) of the sound reflecting surface (see Figure 1F for behavioral results). Both EB and LB, but not C1 or C2, show reliable BOLD activity in calcarine sulcus, typically associated with the processing of visual stimuli. EB shows more BOLD activity in calcarine sulcus than LB. All subjects (except C2) also show BOLD activity along the central sulcus (i.e. Motor Cortex) of the left hemisphere, most likely due to the response related right-hand button press. All subjects also show BOLD activity in the lateral sulcus (i.e. Auditory Complex) of the left and right hemispheres and adjacent and inferior to the right medial frontal sulcus. The former likely reflects the auditory nature of the stimuli. The latter most likely reflects the involvement of higher order cognitive and executive control processes during task performance.
Mentions: Functional MRI revealed reliable blood-oxygen-level dependent (BOLD) activity in auditory cortex as well as in the calcarine sulcus and surrounding regions of “visual” cortex in EB and LB when they listened to recordings of their echolocation clicks and echoes, as compared to silence (Figure 2, top). EB showed stronger activity in the calcarine cortex than did LB, which could reflect EB's much longer use of echolocation and/or his more reliable performance in passive echolocation tasks. Activity in calcarine cortex was entirely absent in C1 and C2 when they listened to the echolocation recordings of EB and LB, although both control subjects showed robust activity in auditory cortex (Figure 2, bottom). This pattern of results was expected based on previous experiments that have measured brain activation in blind and sighted people in response to auditory stimulation as compared to silence [13]–[15].

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