Lavinia Slabu

Electrophysiological evidence for the hierarchical organization of auditory change detection in the human brain

Auditory change detection has been associated with mismatch negativity (MMN), an event-related potential (ERP) occurring at 100-250 ms after the onset of an acoustic change. Yet, single-unit recordings in animals suggest much faster novelty-specific responses in the auditory system. To investigate change detection in a corresponding early time range in humans, we measured the Middle Latency Response (MLR) and MMN during a controlled frequency oddball paradigm. In addition to MMN, an early effect of change detection was observed at about 40 ms after change onset reflected in an enhancement of the Nb component of the MLR. Both MMN and the Nb effect were shown to be free from confounding influences such as differences in refractoriness. This finding implies that early change detection processes exist in humans upstream of MMN generation, which supports the emerging view of a hierarchical organization of change detection expanding along multiple levels of the auditory pathway.

Early change detection in humans as revealed by auditory brainstem and middle-latency evoked potentials.

The ability to detect unexpected novel stimuli is crucial for survival, as it might urge a prompt adaptive response. Human auditory novelty detection has been associated to the mismatch negativity long‐latency auditory‐evoked potential, peaking at 100–200 ms. Yet, recent animal studies showing novelty responses at a very short latency (about 20–30 ms) in individual neurons already at the level of the midbrain and thalamus suggest that novelty detection might be a basic principle of the functional organization of the auditory system, expanding from lower levels in the brainstem along the auditory pathway up to higher‐order areas of the cerebral cortex. To test this suggestion, we here measured auditory brainstem and middle latency response (MLR) to frequency novel stimuli embedded in an oddball sequence. To oversee refractoriness confounds a ‘control block’ was used. The results showed that occasional changes in auditory frequency information were detected as early as 30 ms (Pa waveform of the MLR) after stimulus onset. The control block precluded these effects as resulting merely from refractoriness, altogether supporting the notion of ‘true’ early auditory change detection in humans, matching the latency range of auditory novelty responses described in individual neurons of subhuman species. Our results suggest that auditory change detection of frequency information is a multistage process that occurs at the primary auditory cortex and is transmitted to the higher levels of the auditory pathway.

Multiple time scales of adaptation in the auditory system as revealed by human evoked potentials

Single neurons in the primary auditory cortex of the cat show faster adaptation time constants to short- than long-term stimulus history. This ability to encode the complex past auditory stimulation in multiple time scales would enable the auditory system to generate expectations of the incoming stimuli. Here, we tested whether large neural populations exhibit this ability as well, by recording human auditory evoked potentials (AEP) to pure tones in a sequence embedding short- and long-term aspects of stimulus history. Our results yielded dynamic amplitude modulations of the P2 AEP to stimulus repetition spanning from milliseconds to tens of seconds concurrently, as well as amplitude modulations of the mismatch negativity AEP to regularity violations. A simple linear model of expectancy accounting for both short- and long-term stimulus history described our results, paralleling the behavior of neurons in the primary auditory cortex.

Novelty Detection in the Human Auditory Brainstem

Auditory deviance detection has been associated with a human auditory-evoked potential (AEP), the mismatch negativity, generated in the auditory cortex 100–200 ms from sound change onset. Yet, single-unit recordings in animals suggest much earlier (∼20–40 ms), and anatomically lower (i.e., thalamus and midbrain) deviance detection. In humans, recordings of the scalp middle-latency AEPs have confirmed early (∼30–40 ms) deviance detection. However, involvement of the human auditory brainstem in deviance detection has not yet been demonstrated. Here we recorded the auditory brainstem frequency-following response (FFR) to consonant-vowel stimuli (/ba/, /wa/) in young adults, with stimuli arranged in oddball and reversed oddball blocks (deviant probability, p = 0.2), allowing for the comparison of FFRs to the same physical stimuli presented in different contextual roles. Whereas no effect was observed for the /wa/ syllable, we found for the /ba/ syllable a reduction in the brainstem FFR to deviant stimuli compared with standard ones and to similar stimuli arranged in a control block, with five equiprobable, rarely occurring sounds. These findings demonstrate that the human auditory brainstem is able to encode regularities in the recent auditory past to detect novel events, and confirm the multiple anatomical and temporal scales of human deviance detection.

Involvement of the human midbrain and thalamus in auditory deviance detection

Prompt detection of unexpected changes in the sensory environment is critical for survival. In the auditory domain, the occurrence of a rare stimulus triggers a cascade of neurophysiological events spanning over multiple time-scales. Besides the role of the mismatch negativity (MMN), whose cortical generators are located in supratemporal areas, cumulative evidence suggests that violations of auditory regularities can be detected earlier and lower in the auditory hierarchy. Recent human scalp recordings have shown signatures of auditory mismatch responses at shorter latencies than those of the MMN. Moreover, animal single-unit recordings have demonstrated that rare stimulus changes cause a release from stimulus-specific adaptation in neurons of the primary auditory cortex, the medial geniculate body (MGB), and the inferior colliculus (IC). Although these data suggest that change detection is a pervasive property of the auditory system which may reside upstream cortical sites, direct evidence for the involvement of subcortical stages in the human auditory novelty system is lacking. Using event-related functional magnetic resonance imaging during a frequency oddball paradigm, we here report that auditory deviance detection occurs in the MGB and the IC of healthy human participants. By implementing a random condition controlling for neural refractoriness effects, we show that auditory change detection in these subcortical stations involves the encoding of statistical regularities from the acoustic input. These results provide the first direct evidence of the existence of multiple mismatch detectors nested at different levels along the human ascending auditory pathway.

Decreased BOLD responses in audiovisual processing

Audiovisual processing was studied in a functional magnetic resonance imaging study using the McGurk effect. Perceptual responses and the brain activity patterns were measured as a function of audiovisual delay. In several cortical and subcortical brain areas, BOLD responses correlated negatively with the perception of the McGurk effect. No brain areas with positively correlated BOLD responses were found. This was unexpected as most studies of audiovisual integration use additivity and super additivity – that is, increased BOLD responses after audiovisual stimulation compared with auditory-only and visual-only stimulation – as criteria for audiovisual integration. We argue that brain areas that show decreased BOLD responses that correlate with an integrated audiovisual percept should not be neglected from consideration as possibly involved in audiovisual integration.

Spectrotemporal processing drives fast access to memory traces for spoken words

The Mismatch Negativity (MMN) component of the event-related potentials is generated when a detectable spectrotemporal feature of the incoming sound does not match the sensory model set up by preceding repeated stimuli. MMN is enhanced at frontocentral scalp sites for deviant words when compared to acoustically similar deviant pseudowords, suggesting that automatic access to long-term memory traces for spoken words contributes to MMN generation. Does spectrotemporal feature matching also drive automatic lexical access? To test this, we recorded human auditory event-related potentials (ERPs) to disyllabic spoken words and pseudowords within a passive oddball paradigm. We first aimed at replicating the word-related MMN enhancement effect for Spanish, thereby adding to the available cross-linguistic evidence (e.g., Finnish, English). We then probed its resilience to spectrotemporal perturbation by inserting short (20 ms) and long (120 ms) silent gaps between first and second syllables of deviant and standard stimuli. A significantly enhanced, frontocentrally distributed MMN to deviant words was found for stimuli with no gap. The long gap yielded no deviant word MMN, showing that prior expectations of word form limits in a given language influence deviance detection processes. Crucially, the insertion of a short gap suppressed deviant word MMN enhancement at frontocentral sites. We propose that spectrotemporal point-wise matching constitutes a core mechanism for fast serial computations in audition and language, bridging sensory and long-term memory systems.

The Effect of Slice Orientation on Auditory fMRI at the Level of the Brainstem

Although auditory information is processed in several subcortical nuclei, most fMRI studies focus solely on the auditory cortex and do not take brainstem responses into account. One common difficulty in obtaining clear functional brainstem recordings is due to heartbeat related motion, manifested in the rostro-caudal and in the ventro-dorsal directions in the contraction phase of the heart. The aim of this study was to investigate the effect of slice orientation on auditory functional magnetic resonance imagining (fMRI) measurements with respect to the pattern of brainstem oscillation. Fourteen healthy volunteers listened monaurally to modulated pink noise. Blood oxygenation level dependent (BOLD) contrast was performed with an echo-planar image (EPI) sequence using a 3T MRI system. Three different slice orientations were compared: approximately parallel, at 45°, and orthogonal to the brainstem. The standard deviation of the residuals, the effect size, the median t-values, and the number of activated voxels were calculated to quantify variability in activation between orientations. The data for the inferior colliculi indicated that a slice orientation with a 45° angle to the brainstem yielded the lowest sensitivity to motion (reflected in the standard deviation of the residuals). By contrast, the results did not suggest differences between the three imaging planes on the scanning of the auditory cortex. Findings indicate that the 45° slice orientation is the optimum orientation for accurate measurement at the upper brainstem level.