What is novel in the novelty oddball paradigm? Functional significance of the novelty P3 event-related potential as revealed by independent component analysis

To better understand whether voluntary attention affects how the brain processes novel events, variants of the auditory novelty oddball paradigm were presented to two different groups of human volunteers. One group of subjects (n=16) silently counted rarely presented 'infrequent' tones (p=0.10), interspersed with 'novel' task-irrelevant unique environmental sounds (p=0.10) and frequently presented 'standard' tones (p=0.80). A second group of subjects (n=17) silently counted the 'novel' environmental sounds, the 'infrequent' tones now serving as the task-irrelevant deviant events. Analysis of event-related potentials (ERPs) recorded from 63 scalp channels suggested a spatiotemporal overlap of fronto-central novelty P3 and centro-parietal P3 (P3b) ERP features in both groups. Application of independent component analysis (ICA) to concatenated single trials revealed two independent component clusters that accounted for portions of the novelty P3 and P3b response features, respectively. The P3b-related ICA cluster contributed to the novelty P3 amplitude response to novel environmental sounds. In contrast to the scalp ERPs, the amplitude of the novelty P3 related cluster was not affected by voluntary attention, that is, by the target/nontarget distinction. This result demonstrates the usefulness of ICA for disentangling spatiotemporally overlapping ERP processes and provides evidence that task irrelevance is not a necessary feature of novelty processing.     

The brain's orienting response: An event-related functional magnetic resonance imaging investigation

An important function of the brain's orienting response is to enable the evaluation of novel, environmental events in order to prepare for potential behavioral action. Here, we assessed the event-related hemodynamic (erfMRI) correlates of this phenomenon using unexpected (i.e., novel) environmental sounds presented within the context of an auditory novelty oddball paradigm. In ERP investigations of the novelty oddball, repetition of the identical novel sound leads to habituation of the novelty P3, an ERP sign of the orienting response. Repetition also leads to an enhancement of a subsequent positivity that appears to reflect semantic analysis of the environmental sounds. In this adaptation for erfMRI recording, frequent tones were intermixed randomly with infrequent target tones and equally infrequent novel, environmental sounds. Subjects responded via speeded button press to targets. To assess habituation, some of the environmental sounds were repeated two blocks after their initial presentation. As expected, novel sounds and target tones led to activation of widespread, but somewhat different, neural networks. Contrary to expectation, however, there were no significant areas in which activation was reduced in response to second compared to first presentations of the novel sounds. Conversely, novel sounds relative to target tones engendered activity in the inferior frontal gyrus (BA 45) consistent with semantic analysis of these events. We conclude that a key concomitant of the orienting response is the extraction of meaning, thereby enabling one to determine the significance of the environmental perturbation and take appropriate goal-directed action.     

Optical imaging of temporal integration in human auditory cortex

Behavioral and physiological studies have indicated the existence of a temporal window of auditory integration (TWI), within which similar sounds are perceptually grouped. The current study exploits the combined temporal and spatial resolution of fast optical imaging (the event-related optical signal, EROS) to show that brain activity elicited by sounds within and outside the TWI differs in location and latency. In a previous event-related brain potential (ERP) study [Sable, Gratton, and Fabiani (2003) European Journal of Neuroscience, 17, 2492-2496], we found that the mismatch negativity (MMN; a brain response to acoustic irregularities) elicited by deviations in stimulus onset asynchronies (SOAs) had a unique shape when the deviant SOA was within the TWI. In the present study, we extended these ERP results using EROS. Participants heard trains of five tones. The first four tones had SOAs of 96, 192, 288 or 384 ms. The SOA of the fourth and fifth tones was either the same (standard) or one of the other three (deviant) SOAs. With a deviant SOA of 96 ms, the cortical response was approximately 2 cm anterior to responses to longer SOA deviants, and was followed by a later response that was absent in the other conditions. Similarly to the electrical MMN, the optical mismatch response amplitudes were proportional to the magnitude of interval deviance. These results, in combination with our previous findings, indicate that the temporal integration of sounds is reflected in cortical mismatch responses that differ from the typical response to interval deviance.     

Effects of spatial separation and stimulus probability on the event-related potentials elicited by occasional changes in sound location

The ability to extract information about the spatial location of sounds plays an important role in auditory scene analysis. The present study examined the effects of spatial separation and stimulus probability on auditory event-related potentials (ERPs) to changes in sound location. In Experiment 1, we found that difference waves between ERPs elicited by standard and deviant stimuli showed a biphasic negative-positive response peaking around 126 and 226 ms after deviant onset. The amplitude of both responses increased with decreasing deviant stimulus probability, and increasing stimulus deviance. When the same stimuli were presented with equal probability for all locations (Experiment 2), there were no significant differences in the ERP amplitude and latency. These results suggest that the data reported in Experiment 1 are the result of contextual changes, rather than changes in simple acoustic features. Brain electrical source analyses are consistent with generators located in auditory cortices posterior to Heschel's gyrus. Although occasional changes in sound location elicit earlier peaks than the mismatch negativity (MMN) response reported for other types of deviation, their topographical distribution and behavior are consistent with MMN. The early latency of MMN for changes in sound location is interpreted in the context of an early-warning system to alert the organism to new sound sources in the environment.     

Event-related neuronal responses to acoustic novelty in single-sided deaf cochlear implant users: Initial findings

Objective: A cochlear implant (CI) is an auditory prosthesis restoring profound hearing loss. However, CI-transmitted sounds are degraded compared to normal acoustic hearing. We investigated cortical responses related to CI-degraded against acoustic listening.Methods: Event-related potentials (ERPs) were recorded from eight single-sided deaf CI users who performed a three-stimulus oddball task, separately with their normal hearing ear and CI ear. The oddball tones were occasionally intermitted by novel sounds. ERP responses were compared between electric and acoustic listening for the auditory (N1) and auditory-cognitive (Novelty P3, Target-P3) ERP components.Results: CI-degraded listening was associated with attenuated sensory processing (N1) and with attenuated early cortical responses to acoustic novelty whereas the late cortical responses to acoustic novelty and the target-P3 did not differ between NH and CI ears.Conclusion: The present study replicates the CI-attenuation of Novelty-P3 amplitudes in a within-subject comparison. Further, we show that the CI-attenuation of Novelty-P3 amplitudes extends to early cortical responses to acoustic novelty, but not to late novelty responses.Significance: The dissociation into CI-attenuated P3 early Novelty-P3 amplitudes and CI-unaffected late Novelty-P3 amplitudes represents a cortical fingerprint of CI-degraded listening. It further contributes to general claims of distinct auditory Novelty-P3 sub-components.     

Event-related potential features indexing central auditory discrimination by newborns

Behavioral research has produced little evidence on sound feature discrimination in neonates. Sensory processes underlying sound perception can be studied using the mismatch negativity (MMN) component of auditory event-related potentials (ERPs), which is not contingent on conscious perception and response. Thus, MMN is suitable for studying newborns, who are difficult to obtain behavioral responses from. The present study thus utilized spectrally rich sounds, known to elicit the most replicable MMN in adults, to investigate newborns' preattentive analysis of sound duration and frequency changes. An attempt was also made to control for the obligatory ERP effects on the MMN. Three-partial harmonic tones were presented in Duration and in Frequency oddball conditions to 55 newborns. In the other two, Equiprobable duration and Equiprobable frequency, conditions frequency and duration deviants of the oddball paradigms were presented with equal probabilities among sounds of other durations and frequencies. MMN was elicited in 81% of newborns in Frequency oddball condition and in 78% of newborns in Duration oddball condition. No significant amplitude differences between the duration and frequency MMNs were found, but MMN latency was delayed in Duration condition. The obligatory components seemed to contribute significantly to the deviant-standard difference in Duration but not in Frequency condition. The majority of neonates appear to possess effective sound frequency and duration discrimination mechanisms. Their preattentive sound discrimination is facilitated by spectrally rich sound content. The present findings support a change-detection nature of MMN in neonates; however, sound duration-related obligatory effects need to be taken into account in infant MMN studies.     

Nonuniform impacts of forward suppression on neural responses to preferred stimuli and nonpreferred stimuli in the rat auditory cortex

In natural conditions, human and animals need to extract target sound information from noisy acoustic environments for communication and survival. However, how the contextual environmental sounds impact the tuning of central auditory neurons to target sound source azimuth over a wide range of sound levels is not fully understood. Here, we determined the azimuth‐level response areas (ALRAs) of rat auditory cortex neurons by recording their responses to probe tones varying with levels and sound source azimuths under both quiet (probe alone) and forward masking conditions (preceding noise + probe). In quiet, cortical neurons responded stronger to their preferred stimuli than to their nonpreferred stimuli. In forward masking conditions, an effective preceding noise reduced the extents of the ALRAs and suppressed the neural responses across the ALRAs by decreasing the response strength and lengthening the first‐spike latency. The forward suppressive effect on neural response strength was increased with increasing masker level and decreased with prolonging the time interval between masker and probe. For a portion of cortical neurons studied, the effects of forward suppression on the response strength to preferred stimuli was weaker than those to nonpreferred stimuli, and the recovery from forward suppression of the response strength to preferred stimuli was earlier than that to nonpreferred stimuli. We suggest that this nonuniform forward suppression of neural responses to preferred stimuli and to nonpreferred stimuli is important for cortical neurons to maintain their relative stable preferences for target sound source azimuth and level in noisy acoustic environments.     

Diminished auditory mismatch fields in dyslexic adults

Electroencephalographic studies have demonstrated smaller auditory responses to infrequent deviances of speech and nonspeech sounds in dyslexic than normal-reading subjects. We used a whole-scalp neuromagnetometer to study selectively reactivity of the auditory cortices to sound deviances in 8 dyslexic and 11 normal-reading adults. Within a monotonous sequence of 50-millisecond 1000 Hz binaural tones, tones of 920 and 1080 Hz occurred with 7% probability each. Magnetic mismatch fields, elicited by the stimulus deviances, were diminished in the left hemisphere of the dyslexic subjects. The results indicate deficient change detection in the left auditory cortex of right-handed dyslexic adults.     

Simultaneous storage of two complex temporal sound patterns in auditory sensory memory

We wished to determine whether multiple sound patterns can be simultaneously represented in the temporary auditory buffer (auditory sensory memory), when subjects have no task related to the sounds. To this end we used the mismatch negativity (MMN) event-related potential, an electric brain response elicited when a frequent sound is infrequently replaced by a different sound. The MMN response is based on the presence of the auditory sensory memory trace of the frequent sounds, which exists whether or not these sounds are in the focus of the subject's attention. Subjects watching a movie were presented with sound sequences consisting of two frequent sound patterns, each formed of four different tones and an infrequent pattern consisting of the first two tones of one of the frequent sound pattern and the last two tones of the other frequent sound pattern. The infrequent sound pattern elicited an MMN, indicating that multiple sound patterns are formed at an early, largely automatic stage of auditory processing.     

Event-related brain potentials reveal multiple stages in the perceptual organization of sound

Auditory stream segregation has been suggested to include two distinct processing stages: (1) forming representations for alternative organizations of the acoustic input and (2) choosing one organization for perception after weighing the evidence that supports the different alternatives. The current study tested the possibility that auditory event-related potentials (ERP) could be used to index both stages of the stream-segregation process. Sequences of tones that could be perceived either as a single coherent auditory stream (integrated organization) or as two separate streams of sounds (segregated organization) were presented to subjects. The stimulus configuration encouraged perception to fluctuate between these alternative organizations. Subjects were instructed to continuously indicate whether they perceived one or the other organization of the tone sequence. Occasionally, a tone was omitted from the otherwise regular sequence. This deviance was expected to be processed differently depending on the perceptual organization of the sequence at the time of the omission. We found an early ERP response to omission, which was fully determined by parameters of the stimulation and was not sensitive to the perceived sound organization. In contrast, modulation of two ERP components elicited by the regular tone patterns as well as later responses elicited by deviants correlated with the perceived sound organization. These results suggest that sound organization goes through at least two distinct stages, the first being fully stimulus driven, whereas the second is partly under top-down control.     

An event-related brain potential study of auditory attention in cochlear implant users

ObjectiveCochlear implants (CIs) provide access to the auditory world for deaf individuals. We investigated whether CIs enforce attentional alterations of auditory cortical processing in post-lingually deafened CI users compared to normal-hearing (NH) controls.MethodsEvent-related potentials (ERPs) were recorded in 40 post-lingually deafened CI users and in a group of 40 NH controls using an auditory three-stimulus oddball task, which included frequent standard tones (Standards) and infrequent deviant tones (Targets), as well as infrequently occurring unique sounds (Novels). Participants were exposed twice to the three-stimulus oddball task, once under the instruction to ignore the stimuli (ignore condition), and once under the instruction to respond to infrequently occurring deviant tones (attend condition).ResultsThe allocation of attention to auditory oddball stimuli exerted stronger effects on N1 amplitudes at posterior electrodes in response to Standards and to Targets in CI users than in NH controls. Other ERP amplitudes showed similar attentional modulations in both groups (P2 in response to Standards, N2 in response to Targets and Novels, P3 in response to Targets). We also observed a statistical trend for an attenuated attentional modulation of Novelty P3 amplitudes in CI users compared to NH controls.ConclusionsERP correlates of enhanced CI-mediated auditory attention are confined to the latency range of the auditory N1, suggesting that enhanced attentional modulation during auditory stimulus discrimination occurs primarily in associative auditory cortices of CI users.SignificanceThe present ERP data support the hypothesis of attentional alterations of auditory cortical processing in CI users. These findings may be of clinical relevance for the CI rehabilitation.     

Pre-attentive categorization of vowel formant structure in complex tones

It has been demonstrated that vowel information can be extracted from speech sounds without attention focused on them, despite widely varying non-speech acoustic information in the input. The present study tested whether even complex tones that were constructed based on F0, F1 and F2 vowel frequencies to resemble the defining features of speech sounds, but were not speech, are categorized pre-attentively according to vowel space information. The Mismatch Negativity brain response was elicited by infrequent tokens of the complex tones, showing that the auditory system can pre-attentively categorize speech information on the basis of the minimal, defining auditory features. The human mind extracts the language-relevant information from complex tones despite the non-relevant variation in the sound input.     

Electrical responses reveal the temporal dynamics of brain events during involuntary attention switching

Surviving in the natural environment requires the rapid switching of attention among potentially relevant stimuli. We studied electrophysiologically the involuntary switching time in humans performing a task designed to study brain mechanisms of involuntary attention and distraction (C. Escera et al., 1998, J. Cogn. Neurosci., 10, 590-604). Ten subjects were instructed to discriminate visual stimuli preceded by a task-irrelevant sound, this being either a repetitive tone (P = 0.8) or a distracting sound, i.e. a slightly higher deviant tone (P = 0.1) or an environmental novel sound (P = 0.1). In different conditions, the sounds preceded the visual stimuli by 245 or 355 ms. Deviant tones and novel sounds prolonged reaction times significantly to subsequent visual stimuli by 7.4 (P < 0.02) and 15.2 ms (P < 0.003), respectively. In addition to a mismatch negativity (MMN) and a positive-polarity, 320-ms latency, P3a event-related potential associated, respectively, with detection of the distracting sound and the subsequent orienting of attention to it, a late frontal negative deflection was observed in distracting trials. The peak latency of this brain response from sound onset was 580 ms in the 245-ms condition and 115 ms longer in the 355-ms condition (P < 0.001), peaking consequently at 340 ms from visual stimulus onset, irrespective of the onset of the distracting sound. We suggest that this late frontal negative response may signal over the scalp the process of reallocating attention back to the original task after momentary distraction, and therefore that recovering from distraction may take a similar shifting time as orienting attention involuntarily towards unexpected novelty.     

Early processing of pitch in the human auditory system

Middle‐latency auditory evoked potentials, indicating early cortical processing, elicited by pitch changes and repetitions in pure tones and by complex tones with a missing‐fundamental pitch were recorded in healthy adults ignoring the sounds while watching a silenced movie. Both for the pure and for the missing‐fundamental tones, the Nb middle‐latency response was larger for pitch changes (tones preceded by tones of different pitch) than for pitch repetitions (tones preceded by tones of the same pitch). This Nb enhancement was observed even for missing‐fundamental tones preceded by repeated tones that had a different missing‐fundamental pitch but included all harmonics of the subsequent tone with another missing‐fundamental pitch. This finding rules out the possibility that the Nb enhancement in response to a change in missing‐fundamental pitch was simply attributable to the activity of auditory cortex neurons responding specifically to the harmonics of missing‐fundamental tones. The Nb effect presumably indicates pitch processing at or near the primary auditory cortex, and it was followed by a change‐related enhancement of the N1 response, presumably generated in the secondary auditory cortex. This N1 enhancement might have been caused by a mismatch negativity response overlapping with the N1 response. Processing of missing‐fundamental pitch was also reflected by the distribution of Nb responses. Tones with a higher missing‐fundamental pitch elicited more frontally dominant Nb responses than tones with a lower missing‐fundamental pitch. This effect of pitch, not seen for the pure tones, might indicate that the exact location of the Nb generator source in the auditory cortex depends on the missing‐fundamental pitch of the eliciting tone.     

Event-related potential correlates of sound duration: similar pattern from birth to adulthood.

The effects of sound duration on event-related potentials (ERP) were studied in newborns and adults. Increasing tone duration from 200 to 300 ms led to the enhancement of the N2 peak amplitude, whereas two peaks became distinguishable in the N2 response elicited by 400 ms long tones. The sound-duration related ERP changes most likely reflect contribution from the sustained potential, although the observed results can also be explained by assuming the elicitation of a sound-duration sensitive frontocentrally negative ERP component (duration-sensitive N2; DN2). The pattern of duration-related changes observed in newborn infants was very similar to that in adults, regardless of the structural differences between adult and infant ERPs. The results suggest that sound duration is processed already at birth in a similar way as in adulthood.     

Effects of attention on neuroelectric correlates of auditory stream segregation

A general assumption underlying auditory scene analysis is that the initial grouping of acoustic elements is independent of attention. The effects of attention on auditory stream segregation were investigated by recording event-related potentials (ERPs) while participants either attended to sound stimuli and indicated whether they heard one or two streams or watched a muted movie. The stimuli were pure-tone ABA--patterns that repeated for 10.8 sec with a stimulus onset asynchrony between A and B tones of 100 msec in which the A tone was fixed at 500 Hz, the B tone could be 500, 625, 750, or 1000 Hz, and--was a silence. In both listening conditions, an enhancement of the auditory-evoked response (P1-N1-P2 and N1c) to the B tone varied with Deltaf and correlated with perception of streaming. The ERP from 150 to 250 msec after the beginning of the repeating ABA- patterns became more positive during the course of the trial and was diminished when participants ignored the tones, consistent with behavioral studies indicating that streaming takes several seconds to build up. The N1c enhancement and the buildup over time were larger at right than left temporal electrodes, suggesting a right-hemisphere dominance for stream segregation. Sources in Heschl's gyrus accounted for the ERP modulations related to Deltaf-based segregation and buildup. These findings provide evidence for two cortical mechanisms of streaming: automatic segregation of sounds and attention-dependent buildup process that integrates successive tones within streams over several seconds.     

Electrophysiological evidence of abnormal activation of the cerebral network of involuntary attention in alcoholism.

OBJECTIVE: Increased distractibility is a common impairment in alcoholism, but objective evidence has remained elusive. Here, a task designed to investigate with event-related brain potentials (ERPs) the neural mechanism underlying distraction was used to show abnormal involuntary orienting of attention in chronic alcoholism. METHODS: Fifteen alcoholics and 17 matched healthy controls were instructed to ignore auditory stimuli while concentrating in the discrimination of immediately following visual stimuli. The auditory sequences contained repetitive standard tones occasionally replaced by deviant tones of slightly higher frequency, or by complex novel sounds. RESULTS: Deviant tones and novel sounds distracted visual performance, i.e. increased reaction time to visual stimuli, similarly in patients and controls. Compared to controls, however, alcoholics showed ERP abnormalities, i.e. enhanced P3a amplitudes over the left frontal region, and a positive posterior deflection instead of the frontally distributed reorienting negativity (RON). CONCLUSIONS: The enhanced P3a to novelty and subsequent positive wave instead of RON in alcoholics suggests encoding into working memory of task-irrelevant auditory events and provides neurophysiological markers of impaired involuntary attention mechanisms in chronic alcoholism.     

Tonotopic representation of missing fundamental complex sounds in the human auditory cortex

The N1m component of the auditory evoked magnetic field in response to tones and complex sounds was examined in order to clarify whether the tonotopic representation in the human secondary auditory cortex is based on perceived pitch or the physical frequency spectrum of the sound. The investigated stimulus parameters were the fundamental frequencies (F0 = 250, 500 and 1000 Hz), the spectral composition of the higher harmonics of the missing fundamental sounds (2nd to 5th, 6th to 9th and 10th to 13th harmonic) and the frequencies of pure tones corresponding to F0 and to the lowest component of each complex sound. Tonotopic gradients showed that high frequencies were more medially located than low frequencies for the pure tones and for the centre frequency of the complex tones. Furthermore, in the superior-inferior direction, the tonotopic gradients were different between pure tones and complex sounds. The results were interpreted as reflecting different processing in the auditory cortex for pure tones and complex sounds. This hypothesis was supported by the result of evoked responses to complex sounds having longer latencies. A more pronounced tonotopic representation in the right hemisphere gave evidence for right hemispheric dominance in spectral processing.     

Attentional modulation in the detection of irrelevant deviance: a simultaneous ERP/fMRI study

Little is known about the neural mechanisms that control attentional modulation of deviance detection in the auditory modality. In this study, we manipulated the difficulty of a primary task to test the relation between task difficulty and the detection of infrequent, task-irrelevant deviant (D) tones (1,300 Hz) presented among repetitive standard (S) tones (1,000 Hz). Simultaneous functional magnetic resonance imaging (fMRI)/event-related potentials (ERPs) were recorded from 21 subjects performing a two-alternative forced-choice duration discrimination task (short and long tones of equal probability). The duration of the short tone was always 50 msec. The duration of the long tone was 100 msec in the easy task and 60 msec in the difficult task. As expected, response accuracy decreased and response time (RT) increased in the difficult compared with the easy task. Performance was also poorer for D than for S tones, indicating distraction by task-irrelevant frequency information on trials involving D tones. In the difficult task, an amplitude increase was observed in the difference waves for N1 and P3a, ERP components associated with increased attention to deviant sounds. The mismatch negativity (MMN) response, associated with passive deviant detection, was larger in the easy task, demonstrating the susceptibility of this component to attentional manipulations. The fMRI contrast D > S in the difficult task revealed activation on the right superior temporal gyrus (STG) and extending ventrally into the superior temporal sulcus, suggesting this region's involvement in involuntary attention shifting toward unattended, infrequent sounds. Conversely, passive deviance detection, as reflected by the MMN, was associated with more dorsal activation on the STG. These results are consistent with the view that the dorsal STG region is responsive to mismatches between the memory trace of the standard and the incoming deviant sound, whereas the ventral STG region is activated by involuntary shifts of attention to task-irrelevant auditory features.     

Effects of temporal encoding on auditory object formation: a mismatch negativity study

Analysis of auditory scene relies on the appropriate division of the sensory input into meaningful events. The auditory system uses a sequential grouping strategy to segregate different acoustic events in the time domain. As a result of grouping, the organization of sound is expected to include acoustic events spanning different scales of time. It is unclear, however, at which moment the central auditory system begins to introduce changes in the neural representation of the auditory scene as a result of grouping different information units into a larger acoustic event. The present set of experiments examines this issue by using the mismatch negativity (MMN) component of event-related potentials. The MMN is elicited in response to changes in the previously registered auditory regularity whether or not the subject's attention is focused on the auditory stimuli. By presenting three consecutive pairs of alternating tones in serial stimulus trains, we found that across-train repetitions of the tone elicited the MMN with inter-train intervals up to 240 ms. Beyond this interval, only within-train repetitions of the tone elicited the MMN, suggesting that pairs of tones were bound together into a single acoustic event (i.e., train of six tones) within a temporal window not much longer than 240 ms. Furthermore, a different pattern of responses was seen depending on the position of the deviant event within the train and the frequency distance between the alternating tones. These results suggest that grouping discrete auditory inputs may introduce changes in the neural representation of the auditory scene by applying rules to sounds spanning larger temporal scales.