The lost ability to distinguish between self and other voice following a brain lesion

Abstract

Mechanisms underlying the self/other distinction have been mainly investigated focusing on visual, tactile or proprioceptive cues, whereas very little is known about the contribution of acoustical information. Here the ability to distinguish between self and others' voice is investigated by using a neuropsychological approach. Right (RBD) and left brain damaged (LBD) patients and healthy controls were submitted to a voice discrimination and a voice recognition task. Stimuli were paired words/pseudowords pronounced by the participant, by a familiar or unfamiliar person. In the voice discrimination task, participants had to judge whether two voices were same or different, whereas in the voice recognition task participants had to judge whether their own voice was or was not present. Crucially, differences between patient groups were found. In the discrimination task, only RBD patients were selectively impaired when their own voice was present. By contrast, in the recognition task, both RBD and LBD patients were impaired and showed two different biases: RBD patients misattributed the other's voice to themselves, while LBD patients denied the ownership of their own voice. Thus, two kinds of bias can affect self-voice recognition: we can refuse self-stimuli (voice disownership), or we can misidentify others' stimuli as our own (embodiment of others' voice). Overall, these findings reflect different impairments in self/other distinction both at behavioral and anatomical level, the right hemisphere being involved in voice discrimination and both hemispheres in the voice identity explicit recognition. The finding of selective brain networks dedicated to processing one's own voice demonstrates the relevance of self-related acoustic information in bodily self-representation.

Keywords: Brain damaged patients; Embodiment; LBD patient, left brain damaged patient; Lesion-symptom mapping; RBD patient, right brain damaged patient; Self/other distinction; VLSM, voxel-based lesion-symptom mapping; Voice discrimination; Voice recognition.

Fig. 1

Experimental trial. Example of experimental trial in which two paired voices were subsequently presented.

Fig. 2

Accuracy in voice discrimination and voice recognition tasks as a function of Ownership. The comparison of accuracy (mean percentage of correct responses) in voice discrimination and voice recognition as a function of Ownership (Self, Other) between groups (A) and within group: controls (B), LBD patients (C) and RBD patients (D) are shown. Error bars depict SEMs. Significant differences (p < 0.05) between-groups (2A) and within-group (2B-D) are starred.

Fig. 3

Analysis of errors. The mean of False alarms (FA) and Misses (MISS) expressed as a percentage of error for Controls, left brain damaged (LBD) and right brain damaged (RBD) patients. Error bars depict SEMs. Significant differences (p < 0.05) are starred.

Fig. 4

Overlays lesions plots of right and left brain damaged patients. Overlay of reconstructed lesion plots of right brain damaged (RBD) (A) and left brain damaged (LBD) patients (B) superimposed onto MNI template. The number of overlapping lesions is illustrated by different colours coding from violet (n = 1) to light green (n = 7).

Fig. 5

Representative slices showing the anatomical correlates of voice discrimination and voice recognition. Brain regions significantly associated to self-voice discrimination (A), self-voice recognition (B) and other's voice recognition (C) are represented on the axial, coronal (from left to right) and sagittal plan. All voxels which survived to the permutation correction are displayed (p < 0.05).

Fig. 6

A representation of self-other voice recognition in Controls, left brain damaged (LBD) and right brain damaged (RBD) patients. The figure shows three different scenarios (in Controls, LBD and RBD patients, respectively) in which Self and Other are located at two opposite edges and the double-headed arrow indicates their horizontal continuum. The dot line represents the boundary between self and other. The hypothetical boundary between self and other should be the midpoint of the line in case of equal FA % (erroneous recognition of self-voice) and MISS % (erroneous rejection of self-voice). The deviation with respect to the real midpoint corresponds to the difference between the percentage of FA and MISS rates. A) The green dot line indicates the self/other boundary in Controls (FA minus MISS = −16%). B) The red dot line represents the tendency to deny the ownership of one's own voice (voice disownership) following a left hemisphere lesion (FA minus MISS = −24%). C) The red dot line represents the tendency to misattribute the other's voice to themselves (others' voice embodiment), observed following a right hemisphere lesion (FA minus MISS = 26%). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)