Decay time of the auditory sensory memory trace during wakefulness and REM sleep

In a repetitive auditory stimulus sequence, deviant infrequent tones typically elicit a component of auditory event-related potentials termed mismatch negativity (MMN). The elicitation of MMN is assumed to reflect the existence of a memory trace of the standard stimulus that has a decay time of about 10 s and is strengthened by repetition of the standards. The main aim of the present study was to test the decay time of the sensory memory trace during rapid-eye movement (REM) sleep vs. wakefulness, as indexed by the MMN. Subjects were presented 10 tone trains, separated by 3, 6, or 9 s of silence, during waking and REM sleep. Each train consisted of 9 standards of 1000 Hz and 1 deviant of 2000 Hz that occurred at position 1, 2, 4, or 6. The waking deviants elicited a frontocentral negativity with a scalp topography equivalent to the MMN component. During REM sleep, the negative component showed the same scalp distribution only for the 3-s intertrain interval (ITI). In this brain state, the MMN amplitude was smaller and decreased with prolongation of the ITI. These results suggest a weaker sensory memory trace formation and a premature decay time of such a memory trace during REM sleep as compared with wakefulness.     

Attention and mismatch negativity

The mismatch negativity (MMN) component of the auditory event-related potential (ERP) is elicited by infrequent, physically deviant stimuli in a sequence of frequent homogeneous stimuli (standards). It has been suggested that the MMN is generated by an automatic (attention-independent) neural mismatch process with a memory trace that encodes the physical features of the standard stimulus. The proposed MMN independence of attention was addressed in the present study. Standard stimuli and two types of deviant stimuli, differing from standards either in frequency or intensity, were dichotically presented in random order and at a very rapid rate. The subject attended either to left-or right-ear stimuli, counting the number of a designated type of deviants in that ear. In the present conditions of very strongly focused attention, the MMN was elicited even by frequency change in the ignored input stream, and its amplitude was very similar to that of the MMN elicited by equivalent deviant stimuli (targets) in the attended input stream. In contrast, the MMN to intensity deviation was clearly attenuated in the absence of attention. This effect is, however, probably due to the attention effect on the MMN generator itself rather than the antecedent sensory-analysis and -storing functions.     

Can Echoic Memory Store Two Traces Simultaneously? A Study of Event-Related Brain Potentials

The mismatch negativity, a component of the event-related brain potential elicited by infrequent deviants in sequences of auditory stimuli, is presumably generated by an automatic mismatch process in a mechanism that compares the current stimulus to the trace of the previous one. The present study addressed the possible simultaneous existence of two such traces. Two equiprobable (45% each) frequent stimuli (“standards”), one of 600 Hz and the other of 700 Hz, were presented together with an infrequent (10%), “deviant” stimulus which was of differnet frequency in different blocks. These deviants elicited a mismatch negativity, though a smaller one than that obtained in corresponding blocks with only one standard stimulus. Two aspects of the present results from the blocks with two standard stimuli implicate two parallel stimulus traces in these blocks: 1) deviants elicited a mismatch negativity (MMN) of approximately the same amplitude when preceded by sequences of four identical standards as when preceded by sequences of four stimuli containing both standards; 2) in contrast to the one-standard condition, the magnitude of stimulus deviance did not affect the MMN component elicited by the different deviants.     

Mismatch Negativity Outside Strong Attentional Focus: A Commentary on Woldorff et al. (1991)

Several previous papers have suggested that the mismatch negativity (MMN), an event-related potential (ERP) component specific to stimulus change after repetition, is fully automatic, that is, not affected by attention. Woldorff, Hackley, and Hillyard (1991), however, report that the MMN elicited by an intensity decrement of a repeating stimulus is considerably attenuated when attention is strongly focused on other stimuli. The present commentary attributes most of this effect to attention effects on ERP components other than the MMN but also admits that some attentional reduction of the MMN component indeed occurred. This attenuation was interpreted by Woldorff et al. as indicating suppression of early sensory processing in unattended channels, but this is contraindicated by some very recent data from the present author's laboratory and elsewhere showing that the MMN to frequency change is not attenuated outside a strong attentional focus. Consequently, an alternative explanation is proposed for Woldorff et al.'s important finding.     

Mismatch negativity (MMN): an objective measure of sensory memory and long-lasting memories during sleep.

Sleep, unlike wakefulness, facilitates the internal stimulus generation and hinders the processing of external stimulation. Nevertheless, evidence yielded by physiological studies in animals and event-related potential (ERP) studies in humans suggest that basic functions of the central auditory system are still preserved during sleep. This review is focused on the automatic change-detection function of the auditory system as revealed by a negative ERP component called mismatch negativity (MMN). MMN mainly originates in the auditory cortex, although it also receives an important contribution from subcortical areas (especially at thalamic level), as well as frontal areas. We discuss recent experiments supporting the use of MMN as an objective measure of sensory memory and long-lasting memories not only during wakefulness, but also during sleep. The outcome of the activation of MMN generating system during sleep highly differs from that in waking, especially when there is no previous information about the stimulus sequence in the neuronal network as a result of learning. We discuss these differences in MMN generation in terms of a dynamicist view of the brain that emphasizes the importance of the integration between bottom-up and top-down influences on sensory processing, independently of the processing level in the auditory hierarchy.     

Optimized mismatch negativity paradigm reflects deficits in schizophrenia patients. A combined EEG and MEG study

Mismatch negativity (MMN) and its neuromagnetic analog (MMNm) are event-related brain responses elicited by changes in a sequence of auditory events and indexes early cognitive processing. It consistently detects neural processing deficits in schizophrenia. So far MMN is assessed with different methods (electroencephalography, EEG; magnetoencephalography, MEG) and with different paradigms: the "traditional" oddball design with rare deviants (20%) or the "optimum" design with 50% deviants varying in one of five parameters each. These MMN measures may not reflect one unitary mechanism which is equally affected in schizophrenia. We compared both designs in 12 patients with schizophrenia and controls using MEG and EEG. Automated, observer-independent data analysis rendered the procedures suitable for clinical applications. The optimum design was fastest to detect MMN and MEG had the best signal-to-noise ratio. In addition MMN was mostly reduced in schizophrenia if measured with MEG in the optimum paradigm. Optimized paradigms improve sensitivity and speed for the detection of schizophrenia endophenotypes. Dysfunctions in this disorder may lie primarily in the fast and automatic encoding of stimulus features at the auditory cortex.     

Differential changes in frontal and sub-temporal components of mismatch negativity.

Novel evidence is reported showing changes in the mismatch negativity (MMN) event-related potential (ERP) that followed a different time course in frontal and sub-temporal (mastoid) electrodes. MMN recorded in frontal electrode sites, assumed to originate predominantly in the superior temporal gyrus, showed amplitude enhancement from the first to the second recording block. In contrast, the amplitude of the sub-temporal, mastoid component (termed mismatch positivity, MMP) diminished. In addition to these changes in the MMN elicited by tone duration deviants, there were also significant changes in the ERP to the standard stimulus. The positivity in the standard ERP between 50 and 150 ms increased in bilateral mastoid electrodes but showed no reliable change in frontal electrodes. This suggests that more than one generator underpins the two mismatch components, and that the sub-temporal mismatch component does not only represent a polarity reversal of the main MMN component in the superior temporal gyrus.     

Deviance detection in congruent audiovisual speech: Evidence for implicit integrated audiovisual memory representations

Detection of deviant speech syllables embedded in continuous noise was investigated in an oddball paradigm. Behavioral results showed improvement of detecting and identifying the syllables when congruent visual speech accompanied the utterances. A centrally maximal negative ERP difference wave peaking at approximately 290 ms post-stimulus was elicited by audiovisual but not by auditory- or visual-only task-irrelevant deviant syllables. Whereas the circumstances of the elicitation of this ERP response are similar to those of the mismatch negativity component (MMN and its visual counterpart, vMMN), its scalp distribution differs from that of both unimodal MMNs. Elicitation of an MMN-like ERP response (termed here as the audiovisual MMN: avMMN) suggests that detection of the audiovisual deviants involved integrated audiovisual memory representations. The pattern of behavioral and ERP results suggest that the formation of such cross-modal memory representation does not require voluntary operations and may even proceed for stimuli outside the focus of attention.     

The effects of interstimulus interval on sensory gating and on preattentive auditory memory in the oddball paradigm: Can magnitude of the sensory gating affect preattentive auditory comparison process?

P50, and mismatch negativity (MMN) are components of event-related potentials (ERP) reflecting sensory gating and preattentive auditory memory, respectively. Interstimulus interval (ISI) is an important determinant of the amplitudes of these components and N1. In the present study the interrelation between stimulus gating and preattentive auditory sensory memory were investigated as a function of ISI in 1.5, 2.5 and 3.5 s in 15 healthy volunteered participants. ISI factor affected the N1 peak amplitude significantly. MMN amplitude in 2.5 s ISI was significantly smaller compared to 1.5 and 3.5 s ISI. ISI X stimuli interaction on P50 amplitude was statistically significant. P50 amplitudes to deviant stimuli in 2.5 s ISI were larger than the P50 amplitudes in other ISIs. P50 difference (P50d) waveform amplitude correlated significantly with MMN amplitude. The results suggest that: (i) auditory sensory gating could affect preattentive auditory sensory memory by supplying input to the comparator mechanism; (ii) 2.5 s ISI is important in displaying the sensory gating and preattentive auditory sensory memory relation.     

Categorical perception of lexical tones in Chinese revealed by mismatch negativity

The present study investigated the neurophysiological correlates of categorical perception of Chinese lexical tones in Mandarin Chinese. Relative to standard stimuli, both within- and across-category deviants elicited mismatch negativity (MMN) in bilateral frontal-central recording sites. The MMN elicited in the right sites was marginally larger than in the left sites, which reflects the role of the right hemisphere in acoustic processing. At the same time, relative to within-category deviants, the across-category deviants elicited larger MMN in the left recording sites, reflecting the long-term phonemic traces of lexical tones. These results provide strong neurophysiological evidence in support of categorical perception of lexical tones in Chinese. More important, they demonstrate that acoustic and phonological information is processed in parallel within the MMN time window for the perception of lexical tones. Finally, homologous nonspeech stimuli elicited similar MMN patterns, indicating that lexical tone knowledge influences the perception of nonspeech signals.     

What has MMN revealed about the auditory system in schizophrenia?

Evidence that deficits in early auditory processing occur in schizophrenia was first provided by an ERP study demonstrating that mismatch negativity (MMN) to duration increments is reduced in medicated patients. Our subsequent research, which is reviewed in this paper, demonstrates that duration MMN reduction cannot be attributed to neuroleptic medication, and is specific to schizophrenia. It is not dependent upon the nature of the task used to distract attention away from the auditory modality. Most importantly, a reduced duration MMN in schizophrenia is a replicable result, having been observed in multiple independently-selected groups of patients from two separate laboratories. It also occurs in unaffected first-degree relatives of patients, suggesting that it may be a vulnerability marker of the disorder. The most intriguing questions however, relate to what underpins the reduced MMN to duration increments in schizophrenia and therefore, what it reveals about the nature of the auditory system deficit in this disorder. Three hypotheses are considered here: a pervasive problem in auditory sensory memory; a specific impairment in duration processing; or an abnormality within the window of temporal integration, coincident with the early phase of auditory sensory memory. Our data so far offer preliminary support for the third hypothesis only, although the possibility of a more broadly defined deficit in temporal processing restricted to brief or rapidly-presented auditory stimuli is canvassed.     

Impairment in Mismatch Negativity but not Repetition Suppression in Schizophrenia

Schizophrenia is characterized by impaired auditory-evoked potentials (AEPs), mismatch negativity (MMN), and sensory gating of AEPs to repeated stimuli (repetition suppression, RS). In the predictive modeling framework, MMN and RS reflect encoding of prediction error and model sharpening, respectively. We compared P50, N100, P200 RS, and pitch and duration MMN in 26 participants diagnosed with schizophrenia (SZ) and 26 matched healthy controls (HC), and assessed relationships between MMN, RS, and SZ diagnosis. RS was measured by comparing responses to individual tones presented as 5-tone groups (1 kHz, 75 dB, 50 ms, 5 ms rise/fall times, 330 ms SOA), separated by a 750 ms inter-trial interval. For MMN, the same tones were presented, with occasional pitch (1.2 kHz, 10%) or duration deviants (100 ms, 10%) interspersed. Pitch and duration MMN were reduced in SZ (p?<?0.01). There were no group differences in P50 RS, N100 RS, or P200 RS (p’s?>?0.1). Importantly, although pitch and duration MMN both correlated with RS of AEPs within the MMN time range (p’s?<?0.01), SZ diagnosis predicted MMN over and above RS (p?<?0.05) and shared little variance with RS in prediction of MMN amplitude (tolerance?>?0.93). We suggest that reduced MMN in SZ is related to deficits in encoding prediction error but not repetition suppression.     

Abnormal Complex Auditory Pattern Analysis in Schizophrenia Reflected in an Absent Missing Stimulus Mismatch Negativity

The simple mismatch negativity (MMN) to tones deviating physically (in pitch, loudness, duration, etc.) from repeated standard tones is robustly reduced in schizophrenia. Although generally interpreted to reflect memory or cognitive processes, simple MMN likely contains some activity from non-adapted sensory cells, clouding what process is affected in schizophrenia. Research in healthy participants has demonstrated that MMN can be elicited by deviations from abstract auditory patterns and complex rules that do not cause sensory adaptation. Whether persons with schizophrenia show abnormalities in the complex MMN is unknown. Fourteen schizophrenia participants and 16 matched healthy underwent EEG recording while listening to 400 groups of 6 tones 330 ms apart, separated by 800 ms. Occasional deviant groups were missing the 4th or 6th tone (50 groups each). Healthy participants generated a robust response to a missing but expected tone. The schizophrenia group was significantly impaired in activating the missing stimulus MMN, generating no significant activity at all. Schizophrenia affects the ability of “primitive sensory intelligence” and pre-attentive perceptual mechanisms to form implicit groups in the auditory environment. Importantly, this deficit must relate to abnormalities in abstract complex pattern analysis rather than sensory problems in the disorder. The results indicate a deficit in parsing of the complex auditory scene which likely impacts negatively on successful social navigation in schizophrenia. Knowledge of the location and circuit architecture underlying the true novelty-related MMN and its pathophysiology in schizophrenia will help target future interventions.     

Mismatch negativity to auditory stimulus change recorded directly from the human temporal cortex

Mismatch negativity (MMN) is an event-related potential (ERP) component elicited by any discernible change in a repetitive sound even in the absence of attention. Previous studies have established that MMN is generated by change detection in a process comparing the deviant sensory input with the neural memory trace encoding the physical features of the repetitive sound. In the present study, we recorded MMNs to tonal frequency changes directly from the human temporal cortex of patients with electrodes implanted in the brain for diagnosis and therapy. The intracranially recorded MMN was found to be attention independent and modality specific. It was confined to a rather small area in temporal cortex, which was different from the structures where attention-dependent N2 and P3 responses to the frequency change could be recorded.     

Regularity encoding and deviance detection of frequency modulated sweeps: Human middle‐ and long‐latency auditory evoked potentials

Fast encoding of frequency modulated (FM) sweeps is crucial for communication. In humans, FM sweeps deviating from the acoustic regularity elicit the mismatch negativity (MMN) evoked potential. Yet, direction sensitivity to FM sweeps is found in animals' primary auditory cortex, upstream of MMN sources found in humans. Here, we were interested in whether direction deviants of complex FM sweeps modulated brain responses earlier than MMN. We used a controlled oddball paradigm, and measured the middle latency responses (MLRs) and the MMN. Our results showed a repetition enhancement to the standards at the Pa component of the MLR and a genuine MMN in the later response range. These results show that, early in the cortical hierarchy, the system is sensitive to the physical characteristics of the repetitive stimuli, but a higher‐order mechanism is needed to detect violations of the acoustic regularity.     

The effect of perceptual grouping on the mismatch negativity

The mismatch negativity (MMN) was used as a probe to evaluate changes, with age, of transient auditory memory. Subjects were 16 young (M = 23 years) and 16 old (M = 72 years) people. Standard auditory stimuli were presented in trains of eight tones (1000 Hz) with either a I-s or 8-s intertrain interval (ITI). Occasionally, the first stimulus of a train was replaced with a 1200 Hz tone (deviant). The MMN was recorded while subjects watched a silent movie and ignored the sounds. Both groups of subjects showed an MMN response to deviant stimuli under the 1-s ITI condition, but MMNs were only seen for some subjects under the 8-s ITI condition. After MMN recording, subjects performed a discrimination task to the tones used for recording MMNs. Accuracy for both groups was near 100% at both ITIs. These results suggest that generation of MMN is a function of the perceptual grouping of the acoustical stimuli and that the integrity of perceptual grouping may be maintained with increased age.     

Processing of auditory deviants with changes in one versus two stimulus dimensions

Auditory event-related potentials (ERPs) in response to 50-ms tones were recorded from the human scalp. A standard stimulus ( p = .88) and three different deviants were randomly presented via earphones. There were two one-dimensional deviants (one frequency and one location deviant) and one two-dimensional deviant, with changes in both frequency and location. In one condition, subjects read a book and ignored the auditory stimuli, whereas in another condition they tried to discriminate deviants from standards. In the ignore condition, the two-dimensional deviant elicited an enhanced mismatch negativity (MMN) as compared with the MMNs elicited by the one-dimensional deviants. The temporal and the topographic distributions of the two-dimensional MMNs could be modeled by adding the one-dimensional MMNs. This additivity of the MMNs probably results from the independent activity of separate neural populations generating the frequency and the location MMN. In the attend condition, the deviance-related ERP effects were not additive in the N2b and P3 range, implicating that the neural processes involved in the conscious detection of changes in location and frequency were not independent.     

ERPs and deviance detection: visual mismatch negativity to repeated visual stimuli

Previous studies showed a visual analogue of the mismatch negativity (MMN) event-related potential (ERP), which is elicited by violating some sensory regularity. Separating physical change from violating a regularity, here we show that the visual MMN (vMMN) is elicited by regularity violations that do not involve physical stimulus change. Adult participants were presented with a series of red-black and green-black checkerboard patterns delivered regularly in an RRGGRRGG ... order. Infrequently (p=0.1) this regularity was broken by repeating a stimulus one additional time (e.g. RRGGRRR). ERPs elicited by irregular stimulus repetitions were negatively displaced compared to those elicited both by regular repetition and regular change in two latency ranges: 100-140 ms and 220-260 ms. Whereas the first of these two negative ERP differences appears to be sensitive to stimulus repetition per se, the second difference can be identified as a vMMN response to violating the sequential regularity. Thus, similarly to its auditory counterpart, vMMN reflects deviance-(regularity-violation) rather than change-detection processes.     

Functional features of crossmodal mismatch responses

Research on brain mechanisms of deviance detection and sensory memory trace formation, best indexed by the mismatch negativity, mainly relied on the investigation of responses elicited by auditory stimuli. However, comparable less research reported the mismatch negativity elicited by somatosensory stimuli. More importantly, little is known on the functional features of mismatch deviant and standard responses across different sensory modalities. To directly compare different sensory modalities, we adopted a crossmodal roving paradigm and collected event-related potentials elicited by auditory, non-nociceptive somatosensory, and nociceptive trains of stimuli, during Active and Passive attentional conditions. We applied a topographical segmentation analysis to cluster successive scalp topographies with quasi-stable landscape of significant differences to extract crossmodal mismatch responses. We obtained three main findings. First, across different sensory modalities and attentional conditions, the formation of a standard sensory trace became robust mainly after the second stimulus repetition. Second, the neural representation of a modality deviant stimulus was influenced by the preceding sensory modality. Third, the mismatch negativity significantly covaried between Active and Passive attentional conditions within the same sensory modality, but not between different sensory modalities. These findings provide robust evidence that, while different modalities share a similar process of standard trace formation, the process of deviance detection is largely modality dependent.     

Brain activity from stimuli that are not perceived: Visual mismatch negativity during binocular rivalry suppression

Predictive coding explains visual perception as the result of an interaction between bottom‐up sensory input and top‐down generative models at each level of the visual hierarchy. Evidence for this comes from the visual mismatch negativity (vMMN): a more negative ERP for rare, unpredictable visual stimuli—deviants, than for frequent, predictable visual stimuli—standards. Here, we show that the vMMN does not require conscious experience. We measured the vMMN from monocular luminance‐decrement deviants that were either perceived or not during binocular rivalry dominance or suppression, respectively. We found that both sorts of deviants elicited the vMMN at about 250 ms after stimulus onset, with perceived deviants eliciting a bigger vMMN than not‐perceived deviants. These results show that vMMN occurs in the absence of consciousness, and that consciousness enhances the processing underlying vMMN. We conclude that generative models of visual perception are tested, even when sensory input for those models is not perceived.