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

International audienceThe 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

Involvement of the human midbrain and thalamus in auditory deviance detection

International audiencePrompt 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 timescales. 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 sub-cortical 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

Fast Detection of Unexpected Sound Intensity Decrements as Revealed by Human Evoked Potentials

The detection of deviant sounds is a crucial function of the auditory system and is reflected by the automatically elicited mismatch negativity (MMN), an auditory evoked potential at 100 to 250 ms from stimulus onset. It has recently been shown that rarely occurring frequency and location deviants in an oddball paradigm trigger a more negative response than standard sounds at very early latencies in the middle latency response of the human auditory evoked potential. This fast and early ability of the auditory system is corroborated by the finding of neurons in the animal auditory cortex and subcortical structures, which restore their adapted responsiveness to standard sounds, when a rare change in a sound feature occurs. In this study, we investigated whether the detection of intensity deviants is also reflected at shorter latencies than those of the MMN. Auditory evoked potentials in response to click sounds were analyzed regarding the auditory brain stem response, the middle latency response (MLR) and the MMN. Rare stimuli with a lower intensity level than standard stimuli elicited (in addition to an MMN) a more negative potential in the MLR at the transition from the Na to the Pa component at circa 24 ms from stimulus onset. This finding, together with the studies about frequency and location changes, suggests that the early automatic detection of deviant sounds in an oddball paradigm is a general property of the auditory system

Change detection in children with autism: an auditory event-related fMRI study

Autism involves impairments in communication and social interaction, as well as high levels of repetitive, stereotypic and ritualistic behaviours, and extreme resistance to change. This latter dimension, whilst required for a diagnosis, has received less research attention. We hypothesise that this extreme resistance to change in autism is rooted in atypical processing of unexpected stimuli. We tested this using auditory event-related fMRI to determine regional brain activity associated with passive detection of infrequently occurring frequency-deviant and complex novel sounds in a no-task condition. Participants were twelve 10 to 15-year-old children with autism, and a group of 12 age- and sex-matched healthy controls

Heschl's gyrus is more sensitive to tone level than non-primary auditory cortex

Previous neuroimaging studies generally demonstrate a growth in the cortical response with an increase in sound level. However, the details of the shape and topographic location of such growth remain largely unknown. One limiting methodological factor has been the relatively sparse sampling of sound intensities. Additionally, most studies have either analysed the entire auditory cortex without differentiating primary and non-primary regions or have limited their analyses to Heschl's gyrus (HG). Here, we characterise the pattern of responses to a 300-Hz tone presented in 6-dB steps from 42 to 96 dB sound pressure level as a function of its sound level, within three anatomically defined auditory areas; the primary area, on HG, and two non-primary areas, consisting of a small area lateral to the axis of HG (the anterior lateral area, ALA) and the posterior part of auditory cortex (the planum temporale, PT). Extent and magnitude of auditory activation increased non-linearly with sound level. In HG, the extent and magnitude were more sensitive to increasing level than in ALA and PT. Thus, HG appears to have a larger involvement in sound-level processing than does ALA or PT

Amplitude and frequency-modulated stimuli activate common regions of human auditory cortex

Hall et al. (Hall et al., 2002, Cerebral Cortex 12:140–149) recently showed that pulsed frequency-modulated tones generate considerably higher activation than their unmodulated counterparts in non-primary auditory regions immediately posterior and lateral to Heschl’s gyrus (HG). Here, we use fMRI to explore the type of modulation necessary to evoke such differential activation. Carrier signals were a single tone and a harmonic-complex tone, with a 300 Hz fundamental, that were modulated at a rate of 5 Hz either in frequency, or in amplitude, to create six stimulus conditions (unmodulated, FM, AM). Relative to the silent baseline, the modulated tones, in particular, activated widespread regions of the auditory cortex bilaterally along the supra-temporal plane. When compared with the unmodulated tones, both AM and FM tones generated significantly greater activation in lateral HG and the planum temporale, replicating the previous findings. These activation patterns were largely overlapping, indicating a common sensitivity to both AM and FM. Direct comparisons between AM and FM revealed a higher magnitude of activation in response to the variation in amplitude than in frequency, plus a small part of the posterolateral region in the right hemisphere whose response was specifically AM-, and not FM-, dependent. The dominant pattern of activation was that of co-localized activation by AM and FM, which is consistent with a common neural code for AM and FM within these brain regions

Low-frequency oscillatory correlates of auditory predictive processing in cortical-subcortical networks: a MEG-study

Emerging evidence supports the role of neural oscillations as a mechanism for predictive information processing across large-scale networks. However, the oscillatory signatures underlying auditory mismatch detection and information flow between brain regions remain unclear. To address this issue, we examined the contribution of oscillatory activity at theta/alpha-bands (4–8/8–13 Hz) and assessed directed connectivity in magnetoencephalographic data while 17 human participants were presented with sound sequences containing predictable repetitions and order manipulations that elicited prediction-error responses. We characterized the spectro-temporal properties of neural generators using a minimum-norm approach and assessed directed connectivity using Granger Causality analysis. Mismatching sequences elicited increased theta power and phase-locking in auditory, hippocampal and prefrontal cortices, suggesting that theta-band oscillations underlie prediction-error generation in cortical-subcortical networks. Furthermore, enhanced feedforward theta/alpha-band connectivity was observed in auditory-prefrontal networks during mismatching sequences, while increased feedback connectivity in the alpha-band was observed between hippocampus and auditory regions during predictable sounds. Our findings highlight the involvement of hippocampal theta/alpha-band oscillations towards auditory prediction-error generation and suggest a spectral dissociation between inter-areal feedforward vs. feedback signalling, thus providing novel insights into the oscillatory mechanisms underlying auditory predictive processing

Tuning of Human Modulation Filters Is Carrier-Frequency Dependent

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Some investigations into non passive listening

Our knowledge of the function of the auditory nervous system is based upon a wealth of data obtained, for the most part, in anaesthetised animals. More recently, it has been generally acknowledged that factors such as attention profoundly modulate the activity of sensory systems and this can take place at many levels of processing. Imaging studies, in particular, have revealed the greater activation of auditory areas and areas outside of sensory processing areas when attending to a stimulus. We present here a brief review of the consequences of such non-passive listening and go on to describe some of the experiments we are conducting to investigate them. In imaging studies, using fMRI, we can demonstrate the activation of attention networks that are non-specific to the sensory modality as well as greater and different activation of the areas of the supra-temporal plane that includes primary and secondary auditory areas. The profuse descending connections of the auditory system seem likely to be part of the mechanisms subserving attention to sound. These are generally thought to be largely inactivated by anaesthesia. However, we have been able to demonstrate that even in an anaesthetised preparation, removing the descending control from the cortex leads to quite profound changes in the temporal patterns of activation by sounds in thalamus and inferior colliculus. Some of these effects seem to be specific to the ear of stimulation and affect interaural processing. To bridge these observations we are developing an awake behaving preparation involving freely moving animals in which it will be possible to investigate the effects of consciousness (by contrasting awake and anaesthetized), passive and active listening