Similar EEG Activity Patterns During Experimentally-Induced Auditory Illusions and Veridical Perceptions

Abstract

Hallucinations and illusions are two instances of perceptual experiences illustrating how perception might diverge from external sensory stimulations and be generated or altered based on internal brain states. The occurrence of these phenomena is not constrained to patient populations. Similar experiences can be elicited in healthy subjects by means of suitable experimental procedures. Studying the neural mechanisms underlying these experiences not only has the potential to expand our understanding of the brain's perceptual machinery but also of how it might get impaired. In the current study, we employed an auditory signal detection task to induce auditory illusions by presenting speech snippets at near detection threshold intensity embedded in noise. We investigated the neural correlates of auditory false perceptions by examining the EEG activity preceding the responses in speech absent (false alarm, FA) trials and comparing them to speech present (hit) trials. The results of the comparison of event-related potentials (ERPs) in the activation period vs. baseline revealed the presence of an early negativity (EN) and a late positivity (LP) similar in both hits and FAs, which were absent in misses, correct rejections (CR) and control button presses (BPs). We postulate that the EN and the LP might represent the auditory awareness negativity (AAN) and centro-parietal positivity (CPP) or P300, respectively. The event-related spectral perturbations (ERSPs) exhibited a common power enhancement in low frequencies (<4 Hz) in hits and FAs. The low-frequency power enhancement has been frequently shown to be accompanied with P300 as well as separately being a marker of perceptual awareness, referred to as slow cortical potentials (SCP). Furthermore, the comparison of hits vs. FAs showed a significantly higher LP amplitude and low frequency power in hits compared to FAs. Generally, the observed patterns in the present results resembled some of the major neural correlates associated with perceptual awareness in previous studies. Our findings provide evidence that the neural correlates associated with conscious perception, can be elicited in similar ways in both presence and absence of externally presented sensory stimuli. The present findings did not reveal any pre-stimulus alpha and beta modulations distinguishing conscious vs. unconscious perceptions.

Keywords: CPP; P300; SCP; auditory awareness negativity; auditory illusions; auditory perception; late positivity; signal detection.

FIGURE 1

Experimental design and stimuli. (A) Timeline of the experimental session. At the beginning, each individual’s hearing threshold for the masking noise was estimated (∼3 min). The noise intensity level was set to 40 dB HL and the speech snippet intensity leading to a 70.7% correct detection rate was estimated in the next part (∼6 min). The speech intensity was set within ± 1.5 dB range of the detection threshold. A short practice task was implemented before the main experiment at which positive feedback was provided for correct detections and negative feedback for missed detections of the stimuli (2 min). Afterward, the main signal detection experiment started which was divided into three blocks with self-paced breaks in between while EEG was recorded. Finally, a subset of subjects took part in an additional task of presseing the button as a control condition (more detailed information can be found in “Materials and Methods” section). (B) The amplitude of speech and noise stimuli over a sample 50 s sub-period of the total block duration. The same ISI pattern was repeated twelve times in the course of each experimental block (10 min). (C) Power spectral density (PSD) of the speech-shaped-noise (SSN) used in the experiment in comparison to white and pink noise. SSN was used as the masking noise in the present study.

FIGURE 2

(A) The reaction time (RT) histogram, normalized to produce an estimation of the probability density function (PDF) and Gaussian smoothed distribution for all subjects relative to stimulus presentation. (B) Criteria for categorizing the trials. A hit is identified when a response is given to a stimulus in the time interval between 300 and 1,800 ms. If no response is given to the stimulus up to 3,600 ms, this trial is labeled as a miss. Responses that occur in a time window lasting from 3,600 ms after stimulus presentation until the onset of the next stimulus denote FA trials. (C) The number of hits, misses and FAs across the subjects. (D) The box plot of the number of hits, misses and FAs for all subjects. On each box, the central mark indicates the median, and the bottom and top edges of the box indicate the 25th and 75th percentiles, respectively. The whiskers extend to the most extreme data points not considered outliers.

FIGURE 3

Group-averaged ERP, ERSP and spectral profiles for different frequency bands for hits and FAs. Time is denoted on the x-axis in seconds. The left column depicts the hits aligned to the stimulus onset, the middle column illustrates the data corresponding to hits aligned to the response execution and the right column exhibits FAs (aligned to the response time). The dashed vertical line marks the median reaction time in the left column and the median stimulus onset in the middle column. The scalp topographies with marked electrodes as filled circles represent the significant cluster distributions (negative difference: blue outer circle, positive difference: red outer circle). The rest of the scalp topography maps represent the spatial spread of the half width at half prominence of the illustrated peak or trough in the left part of the panel (also color coded with the outer circle). (A) Baseline corrected ERPs (left: –1.3 to –1.1 s, middle and right: –3.1 to –2.9 s). The shaded areas around the ERPs denote the standard error of the mean. The shaded intervals in light red and blue mark the significant interval with positive and negative differences with respect to baseline. (B,C) ERSPs for each trial group are plotted for a representative channel. Frequency (in Hz) is shown on the y-axis. The plotted values are in units of the power change relative to the baseline power. The baseline time range at each frequency is the interval between the minimum latency illustrated in the plot and the black curve. The time range between the curve and the straight line to its right marks the marginal boundary between the baseline and the activation intervals accounting for the temporal smearing caused by the wavelets’ temporal width. The significant cluster for the plotted electrode is marked by the black contour. (B) Top row: ERSPs are plotted for the frequency range of 1–7 Hz for electrode “Pz” as a representative of the time-frequency spectral pattern. Bottom row: The Spectral power traces plotted for SCP range. (C) Top row: average ERSPs are plotted for the frequency range of 7–30 Hz for electrodes “C3” and “C4” as a representative of the time-frequency spectral pattern. Bottom row: The Spectral power traces plotted separately for alpha and beta frequency bands.

FIGURE 4

Comparison of ERPs and ERSPs (1–7 Hz) between different trial types. Time is denoted on the x-axis in seconds. ERSP plots reflect differences between the two conditions. All the plots represent the signals at electrode “Pz.” The shaded intervals in light red and blue mark the significant interval with positive and negative differences between the two conditions. The topographies on the right of the ERPs represent the scalp distribution of the voltages corresponding to the two conditions separately (top two rows of topographies) at the time with strongest negative (left) and strongest positive differences (right) and the differences between conditions (bottom row of topographies). The marked electrodes with filled circles are part of the significant cluster. The black contour in the ERSPs marks the significant cluster and the topography maps show the scalp distribution of the significant cluster. (A) Hit-miss, aligned to stimulus-onset (N = 16). The dashed vertical line marks the median reaction time. (B) FA-CR, aligned to response time (N = 16) (C) Hit-FA, aligned to response time (N = 16). The dashed vertical line marks the negative median reaction time (D) FA-BP, aligned to response time (N = 7).

FIGURE 5

Spatial correlation between topographies of ERP Components in stimulus-aligned and response-aligned hits for (A) the early negativity and (B) the late positivity. Topographies in the upper row correspond to response-aligned hits and in the lower row to stimulus-aligned hits. Scalp topographies of the components were highly correlated in stimulus-aligned and response-aligned hits across most of the subjects.

FIGURE 6

Spatial correlation between topographies of ERP Components in response-aligned hits and FAs for (A) the early negativity and (B) the late positivity. Topographies in the upper row correspond to response-aligned hits and in the lower row to FAs. Scalp topographies of the components were highly correlated in response-aligned hits and FAs across most of the subjects.