The neural activity of auditory conscious perception

Abstract

Although recent work has made headway in understanding the neural temporospatial dynamics of conscious perception, much of that work has focused on visual paradigms. To determine whether there are shared mechanisms for perceptual consciousness across sensory modalities, here we test within the auditory domain. Participants completed an auditory threshold task while undergoing intracranial electroencephalography. Recordings from >2,800 grey matter electrodes were analyzed for broadband gamma power (a range which reflects local neural activity). For perceived trials, we find nearly simultaneous activity in early auditory regions, the right caudal middle frontal gyrus, and the non-auditory thalamus; followed by a wave of activity that sweeps through auditory association regions into parietal and frontal cortices. For not perceived trials, significant activity is restricted to early auditory regions. These findings show the cortical and subcortical networks involved in auditory perception are similar to those observed with vision, suggesting shared mechanisms for conscious perception.

Keywords: Auditory perception; Awareness; Consciousness; ECOG; EEG; Electrophysiology; Hearing; Intracranial electroencephalography; Thalamus.

Fig. 1.. Auditory threshold task and behavior.

(A) Single trial of auditory perceptual threshold task. A 3–5 second prestimulus interval was presented, consisting of auditory white noise played concurrently with visual noise with a central, white fixation cross displayed on a laptop. Following this, in 86 % of trials, an auditory target stimulus (waterdrop, whistle or ‘laser’) was played at the participant’s previously-calibrated 50 % detection threshold; in the remaining 14 % of trials, no target stimulus was played (‘blanks’). Target (or blank) presentation was followed by a post-stimulus interval of 3, 4 or 5 s of visual and auditory noise. Following the post-stimulus interval, two non-timed, forced-choice questions were displayed on the laptop screen regarding (1) whether the participant heard a target stimulus (‘perception question’; shown here with 1 for Yes and 2 for No, but this was randomized by participant), and (2) the identity of the target stimulus (‘identification question’). Following button press for the second question, the next trial immediately began with a total of 50 trials per run. (B) Responses to perception question. In trials in which a target sound was present, 58.8 % of trials were reported as heard; in trials without a target sound (‘blanks’), 8.5 % of trials were reported as heard. Error bars indicate SEM. (C) Responses to identification question. For trials in which a target sound was presented and heard, targets were correctly identified in 89.2 % of trials. In contrast, participants correctly identified only 40.2 % of the target sounds when they were reported as not heard. Outlined in yellow are the validated and confirmed “perceived” and “not perceived” trials analyzed in this study, heretofore referred to simply as “Perceived” and “Not Perceived.” N = 31 participants.

Fig. 2.. Visualizations of electrode distribution and parcellation.

(A) Distribution of electrodes in the 31 study participants. Lateral, medial, ventral and posterior views of both hemispheres are shown on an inflated brain. Each participant’s gray matter electrodes are colored by a different color and displayed at the closest vertex. Background color (on inflated brain) display the number of participants contributing to the signal at each location on the brain surface. Total number of grey matter electrodes across all subjects = 2805. (B) Example of the 80-parcel bilateral parcellation map (40 parcels per hemisphere) generated using k-mean clustering algorithm. 100 such parcellation maps were constructed to ensure statistical findings were robust to boundaries of parcellations (see Methods).

Fig. 3.. Statistically significant gamma power changes in Perceived and Not Perceived trials for threshold auditory stimuli.

(A) Perceived trials. Gamma power increases were first observed in the right caudal frontal gyrus (overlapping with the frontal eye fields) and soon thereafter in bilateral early auditory regions and central thalamic areas (~100–200 ms after stimulus presentation). Increases spread into higher order auditory and frontal regions, and persisted until approximately 750 ms post stimulus. (B) Not Perceived trials. Significant activity was restricted to the left early auditory and auditory adjacent regions. However, it persisted from ~100 to 750 ms post stimulus onset. Vertices are only shown if they were found to be statistically significant during that timepoint; color reflects weighted z-scored gamma power. N = 31 participants. For display of all 100 ms time points at 25 ms intervals see Supplementary Presentation S1.

Fig. 4.. Statistically significant gamma power changes in Perceived - Not Perceived trials for threshold auditory stimuli.

Differences in gamma power were first observed in the right caudal frontal gyrus (overlapping with the frontal eye fields), bilateral early auditory regions and central thalamic areas with greater increases for Perceived trials. The greater increases for Perceived trials then spread into higher order auditory and frontal regions, and persisted until approximately 750 ms post stimulus. Relative decreases were noted to be greater mainly for Perceived trials in ventrolateral regions of the right prefrontal cortex. Vertices are only shown if they were found to be statistically significant during that timepoint; color reflects weighted z-scored gamma power. Same data and participants as in Fig. 3. N = 31 participants. For display of all 100 ms time points at 25 ms intervals see Supplementary Presentation S1.

Fig. 5.. Gamma power time courses of 6 ROIS.

(A) Six anatomical regions of interest (ROIs) were selected. The ROIs include early auditory regions, the caudal middle frontal gyrus (MFG), the thalamus, the anterior insula, the inferior frontal gyrus (IFG) pars opercularis and the supramarginal gyrus. Their locations are displayed on lateral (left and right) and medial (right) views on a brain. Electrodes were only present in the right thalamus, and so the left is not displayed. (B) Perceived – Not Perceived Analysis. Upper traces in each plot show average activity (weighted z-score) of all vertices within the ROI that achieved significance at any time point. Lower traces show the proportion of vertices that were significant (sig. vert.) for each time bin. Vertical colored dotted lines indicate the time bin during which 50 % or more of significant vertices first achieved significance for the ROI in the left (blue) and right (red) hemisphere. The earliest significant changes were observed in early auditory, caudal MFG and thalamic regions (top row); slightly later changes in gamma power were observed in anterior insula, IFG pars opercularis and the supramarginal gyrus. Vertical black dashed lines and yellow shaded regions, respectively, indicate onset timing and duration of the 75 ms auditory stimulus. Same data and participants as in Fig. 4 (N = 31).

Fig. 6.. Detect, pulse, switch, and wave hypothesis.

Sequence of neural mechanisms proposed to produce conscious awareness of an external auditory stimulus. Importantly, these are not necessarily discrete steps, but likely have overlapping time scales. (1) Detection is a signal observed in early auditory sensory regions, the FEF and possibly other areas. (2) The pulse is a facilitatory signal that originates in subcortical arousal regions such as the intralaminar thalamus, with widespread cortical connectivity. (3) The switch shows a decreased activity in default mode regions. (4) A wave of activity sweeps from hierarchically early sensory areas into higher order association areas. Red designates increased activity; blue designates reduced activity. Question marks designate areas likely to play a role in signal detection, interacting with primary sensory cortex. In the “pulse”, information flows outwards from a centralized set of subcortical arousal regions (arrows). In the “wave,” information flows from hierarchically lower sensory areas through sequential areas of higher association cortex and memory areas. Adapted with permission from Blumenfeld 2023.