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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.

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BOLD activity in the cerebellum.Data are shown in neurological convention, i.e. left is left. Activity in the cerebellum was analyzed in stereotaxic space [49]. To evaluate significance of activity we used the same voxelwise significance thresholds as for cortical surface analyses for each participant. However, because the number of voxels in volume space differed from the number of vertices in surface space for each participant, the Bonferroni corrected significance level differs between cortex and cerebellum (compare Figure 2). To increase accuracy, cerebellar structures for each participant were identified based on anatomical landmarks. Structures were labeled according to the nomenclature developed by [26]. Left panel: BOLD activity while participants listened to recordings of 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). Right Panel: Contrast between BOLD activations for recordings containing echoes from objects and recordings that did not contain such echoes. Data are not shown if no significant activity was found (empty cells in table).
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pone-0020162-g006: BOLD activity in the cerebellum.Data are shown in neurological convention, i.e. left is left. Activity in the cerebellum was analyzed in stereotaxic space [49]. To evaluate significance of activity we used the same voxelwise significance thresholds as for cortical surface analyses for each participant. However, because the number of voxels in volume space differed from the number of vertices in surface space for each participant, the Bonferroni corrected significance level differs between cortex and cerebellum (compare Figure 2). To increase accuracy, cerebellar structures for each participant were identified based on anatomical landmarks. Structures were labeled according to the nomenclature developed by [26]. Left panel: BOLD activity while participants listened to recordings of 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). Right Panel: Contrast between BOLD activations for recordings containing echoes from objects and recordings that did not contain such echoes. Data are not shown if no significant activity was found (empty cells in table).

Mentions: When EB and LB listened to recordings of their echolocation clicks and echoes, as compared to silence, they both showed significant BOLD activity in lobules VI and VIII (Figure 6, left). A similar pattern was observed in the two sighted participants (Figure 6, left). In other words, lobules VI and VIII appeared to be more active when all our participants listened to auditory stimuli as compared to silence. This pattern of activity is generally consistent with results that link activity in lobules VI and VIII to auditory sensory processing [25]. We also found robust activation in left lobule VIIAt/Crus II in all participants (Figure 6, left). To date, lobule VIIAt/Crus II has not been implicated in sensory processing, but it has been suggested that it is part of a non-motor loop involving Brodmann area 46 in prefrontal cortex [24]. Consistent with this idea, the activation in left lobule VIIAt/Crus II coincides with activity adjacent and inferior to right medial frontal sulcus in all participants (compare Figure 2). Finally, both EB and LB showed robust activation in vermal lobule VI and lobule X, both of which have been linked to visual sensory processing [25]. Interestingly, however, C2 also shows activity in vermal lobule VI and close to lobule X. In summary, for the comparison of echolocation to silence, we found reliable activation in the cerebellum, but this activation did not clearly distinguish between EB and LB on the one hand, and C1 and C2 on the other.


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

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

BOLD activity in the cerebellum.Data are shown in neurological convention, i.e. left is left. Activity in the cerebellum was analyzed in stereotaxic space [49]. To evaluate significance of activity we used the same voxelwise significance thresholds as for cortical surface analyses for each participant. However, because the number of voxels in volume space differed from the number of vertices in surface space for each participant, the Bonferroni corrected significance level differs between cortex and cerebellum (compare Figure 2). To increase accuracy, cerebellar structures for each participant were identified based on anatomical landmarks. Structures were labeled according to the nomenclature developed by [26]. Left panel: BOLD activity while participants listened to recordings of 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). Right Panel: Contrast between BOLD activations for recordings containing echoes from objects and recordings that did not contain such echoes. Data are not shown if no significant activity was found (empty cells in table).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3102086&req=5

pone-0020162-g006: BOLD activity in the cerebellum.Data are shown in neurological convention, i.e. left is left. Activity in the cerebellum was analyzed in stereotaxic space [49]. To evaluate significance of activity we used the same voxelwise significance thresholds as for cortical surface analyses for each participant. However, because the number of voxels in volume space differed from the number of vertices in surface space for each participant, the Bonferroni corrected significance level differs between cortex and cerebellum (compare Figure 2). To increase accuracy, cerebellar structures for each participant were identified based on anatomical landmarks. Structures were labeled according to the nomenclature developed by [26]. Left panel: BOLD activity while participants listened to recordings of 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). Right Panel: Contrast between BOLD activations for recordings containing echoes from objects and recordings that did not contain such echoes. Data are not shown if no significant activity was found (empty cells in table).
Mentions: When EB and LB listened to recordings of their echolocation clicks and echoes, as compared to silence, they both showed significant BOLD activity in lobules VI and VIII (Figure 6, left). A similar pattern was observed in the two sighted participants (Figure 6, left). In other words, lobules VI and VIII appeared to be more active when all our participants listened to auditory stimuli as compared to silence. This pattern of activity is generally consistent with results that link activity in lobules VI and VIII to auditory sensory processing [25]. We also found robust activation in left lobule VIIAt/Crus II in all participants (Figure 6, left). To date, lobule VIIAt/Crus II has not been implicated in sensory processing, but it has been suggested that it is part of a non-motor loop involving Brodmann area 46 in prefrontal cortex [24]. Consistent with this idea, the activation in left lobule VIIAt/Crus II coincides with activity adjacent and inferior to right medial frontal sulcus in all participants (compare Figure 2). Finally, both EB and LB showed robust activation in vermal lobule VI and lobule X, both of which have been linked to visual sensory processing [25]. Interestingly, however, C2 also shows activity in vermal lobule VI and close to lobule X. In summary, for the comparison of echolocation to silence, we found reliable activation in the cerebellum, but this activation did not clearly distinguish between EB and LB on the one hand, and C1 and C2 on the other.

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