Vestigial auriculomotor activity indicates the direction of auditory attention in humans

  1. Daniel J Strauss  Is a corresponding author
  2. Farah I Corona-Strauss
  3. Andreas Schroeer
  4. Philipp Flotho
  5. Ronny Hannemann
  6. Steven A Hackley
  1. Systems Neuroscience and Neurotechnology Unit, Faculty of Medicine, Saarland University & School of Engineering, htw saar, Germany
  2. Audiological Research Unit, Sivantos GmbH, Germany
  3. Clinical and Cognitive Neuroscience Laboratory, Department of Psychological Sciences, University of Missouri, United States
12 figures, 3 videos and 2 additional files

Figures

Experimental setup.

(A) Four loudspeakers presented novel sounds (Exp. 1) or stories (Exp. 2) at 30° to the left or right of fixation or behind the interaural axis. Instructions, text, or fixation cross was displayed …

Figure 2 with 1 supplement
Experiment 1.

Grand average (N = 28) of the baseline corrected and normalized event-related electromyograms at the four auricular muscles for the recordings ipsilateral (left panel) and contralateral (right …

Figure 2—figure supplement 1
Analysis of video recordings from one participant who exhibited submillimeter pinna displacements in response to stimulation in Experiment 1 (Exogenous Attention).

Given the time ti of a stimulus, we analyzed 2s video segments with pre-stimulus onset t0i=ti0.25s. The frames at t00 of the first stimulus (direction +120°) of the left and right recordings were manually …

Figure 3 with 3 supplements
Experiment 1 – Responses of the PAM to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots. …

Figure 3—figure supplement 1
Experiment 1 – Responses of the AAM to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 3—figure supplement 2
Experiment 1 – Responses of the SAM to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 3—figure supplement 3
Experiment 1 – Responses of the TAM to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 4 with 3 supplements
Experiment 1 – Intrasubject variability of the PAM: Mean and standard deviations of the phasic responses 50 - 300 ms) of every participant.

Top panels: responses to the front speakers. Bottom panels: responses to the back speakers. Left panels: Responses of the younger adults. Right panels: responses of the older adults. Blue represents …

Figure 4—figure supplement 1
Experiment 1 – Intrasubject variability of the AAM: Mean and standard deviations of the phasic responses ( 50 - 300 ms) of every participant.

Top panels: responses to the front speakers. Bottom panels: responses to the back speakers. Left panels: Responses of the younger adults. Right panels: responses of the older adults. Blue represents …

Figure 4—figure supplement 2
Experiment 1 – Intrasubject variability of the SAM: Mean and standard deviations of the phasic responses (50 -300 ms) of every participant.

Top panels: responses to the front speakers. Bottom panels: responses to the back speakers. Left panels: Responses of the younger adults. Right panels: responses of the older adults. Blue represents …

Figure 4—figure supplement 3
Experiment 1 – Intrasubject variability of the TAM: Mean and standard deviations of the phasic responses ( 50 - 300 ms) of every participant.

Top panels: responses to the front speakers. Bottom panels: responses to the back speakers. Left panels: Responses of the younger adults. Right panels: responses of the older adults. Blue represents …

Figure 5 with 2 supplements
Experiment 2.

Grand average of the PAM, AAM, and SAM activity when stories were played from the front (top) and back speakers (bottom). Shown is the normalized (total) energy of the left/right recording channels …

Figure 5—figure supplement 1
Grand average of the PAM, AAM, and SAM activity when stories were played from front (± 30°) and back speakers (± 120°).

The normalized total energy in each octave-frequency subband is plotted for the left/right recording channels (in the conventional dyadic order) during attention to the left or right story, along …

Figure 5—figure supplement 2
Analogous to Figure 5 and Figure 6, respectively, in the main text but for frequency band 5 (37.5 – 75 Hz): Grand average of the PAM, AAM, and SAM activity when stories were played from the back speakers (± 120°).

Top: normalized total energy of the left/right recording channels when attending to the left or right story (bars represent the standard error). A significant interaction of recording channel and …

Experiment 2.

Time–resolved activity (each sampling point represents the energy induced in consecutive 10 s segments) after pooling the ipsi– and contralateral signals with a segment–wise normalization for the …

Figure 7 with 9 supplements
Experiment 1: Averaged horizontal EOG activity at around the time of stimulation from the back speakers, showing an apparent absence of systematic shifts in gaze direction: Top panels: Every row corresponds to the averaged response of one participant.

Gaze angle is encoded in color, such that positive values (yellow) indicate rightward eye movements/positive angles. The top rows (1-16) represent younger adult participants; the bottom rows …

Figure 7—figure supplement 1
Macrosaccades during reading in Experiment one as recorded by means of horizontal EOG (black line) along with time-synchronized EMG from left and right PAM (blue and orange lines, respectively).

This participant (# 15) had large, clear PAM responses. Different trials are shown in the four panels. Note that muscle activations occur without saccades and large saccades occur without muscle …

Figure 7—figure supplement 2
Boxplots of EOG signals from all subjects in Experiment 1.

Every stimulus presentation, including 3 s long pre– and poststimulus intervals, were included. Blue dots mark the median, outliers (data points beyond 1.5 x interquartile range) are displayed in …

Figure 7—figure supplement 3
Density of detected macrosaccades during Experiment 1.

Top plot: Every line corresponds to one stimulus presentation (trials). Detected macrosaccades are marked by black dots. Across all subjects, 1008 stimuli were presented. Bottom plot: Histogram of …

Figure 7—figure supplement 4
Experiment 1 – Responses of the M. sternocleidomastoideus (M.SCM) to stimuli from the front speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 7—figure supplement 5
Experiment 1 – Responses of the M. sternocleidomastoideus (M.SCM) to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 7—figure supplement 6
Experiment 1 – Responses of the frontalis muscle to stimuli from the front speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 7—figure supplement 7
Experiment 1 – Responses of the frontalis muscle to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 7—figure supplement 8
Experiment 1 – Responses of the zygomaticus muscle to stimuli from the front speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 7—figure supplement 9
Experiment 1 – Responses of the zygomaticus muscle to stimuli from the back speakers, showing intersubject variability: Top panels: Every row corresponds to the averaged response of one participant.

Amplitude is encoded in color. The top rows (1-16) represent younger adult participants; the bottom rows (17-28), older adults. Bottom panels: Mean and standard deviation based on the above plots.

Figure 8 with 2 supplements
Experiment 2: Intrasubject variability of the horizontal EOG: Mean and standard deviations of the EOG during the complete trial of every participant.

Top panels: attending the front speakers. Bottom panels: attending the back speakers. Left panels: younger adults. Right panels: older adults. Blue represents the EOG when attending the left, red …

Figure 8—figure supplement 1
Time-resolved activity (sampling points represent the energy within consecutive 10 s segments) after pooling the ipsi- and contralateral EOG signals for the front (left) and back speakers (right) in Experiment 2.
Figure 8—figure supplement 2
Grand average of the zygomaticus and frontalis muscle activity when stories were played from the front (top row) and back speakers (bottom row) in Experiment 2.

Shown is the normalized (total) energy of the left/right recording channels during attention to the left or right story (bars represent the standard error). There was no significant interaction of …

Author response image 1
Macrosaccades in the EOG (black line) during reading in Experiment 1 for subject 15 as example (a subject with large, clear PAM activations).

It is noticeable that the muscle activations are not linked to the macrosaccades.

Author response image 2
Left/right decoding performance for a conjoint classification of PAM/SAM EMG using an individualized decoding scheme in Experiment 2.
Author response image 3
Left/right decoding performance for a conjoint classification of PAM/SAM EMG using an(non-individualized) decoding scheme in Experiment 2 with a leave-one-participant-out cross validation.
Author response image 4
Left/right decoding performance for a conjoint classification of PAM/AAM/SAM/TAM EMG using an (non-individualized) decoding scheme in Experiment 1 with a leave-one-participant-out cross validation.

Videos

Video 1
Experiment 1 –Ear movement example from a trial with a novel sound at the right posterior speaker in Experiment 1.

The right half of the display portrays evoked movements of the ipsilateral pinna in three ways. The large video clip of the pinna uses digital magnification to render the overall pattern of movement …

Video 2
Experiment 1 –The right ear example from the previous video, but with four different videos in sequence.

The first video of the sequence shows the raw recording (without digital magnification). The second video shows the digitally magnified motion, the third video shows the magnified motion with color …

Video 3
Experiment 2 –Ear movement example from a participant who exhibited exceptionally large, long-lasting involuntary auricular muscle activations and ear motion during the endogenous attention task in Experiment 2.

The attention of the participant was directed to the story played from the posterior right speaker. The organization of the plots and co-registration is as in Video 1. However, this time the raw …

Additional files

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