Intracortical responses in human and monkey primary auditory cortex support a temporal processing mechanism for encoding of the voice onset time phonetic parameter

This study tests the hypothesis that temporal response patterns in primary auditory cortex are potentially relevant for voice onset time (VOT) encoding in two related experiments. The first experiment investigates whether temporal responses reflecting VOT are modulated in a way that can account for boundary shifts that occur with changes in first formant (F1) frequency, and by extension, consonant place of articulation. Evoked potentials recorded from Heschl's gyrus in a patient undergoing epilepsy surgery evaluation are examined. Representation of VOT varies in a manner that reflects the spectral composition of the syllables and the underlying tonotopic organization. Activity patterns averaged across extended regions of Heschl's gyrus parallel changes in the subject's perceptual boundaries. The second experiment investigates whether the physiological boundary for detecting the sequence of two acoustic elements parallels the psychoacoustic result of approximately 20 ms. Population responses evoked by two-tone complexes with variable tone onset times (TOTs) in primary auditory cortex of the monkey are examined. Onset responses evoked by both the first and second tones are detected at a TOT separation as short as 20 ms. Overall, parallels between perceptual and physiological results support the relevance of a population-based temporal processing mechanism for VOT encoding.     

Specialization of left auditory cortex for speech perception in man depends on temporal coding.

Speech perception requires cortical mechanisms capable of analysing and encoding successive spectral (frequency) changes in the acoustic signal. To study temporal speech processing in the human auditory cortex, we recorded intracerebral evoked potentials to syllables in right and left human auditory cortices including Heschl's gyrus (HG), planum temporale (PT) and the posterior part of superior temporal gyrus (area 22). Natural voiced /ba/, /da/, /ga/) and voiceless (/pa/, /ta/, /ka/) syllables, spoken by a native French speaker, were used to study the processing of a specific temporally based acoustico-phonetic feature, the voice onset time (VOT). This acoustic feature is present in nearly all languages, and it is the VOT that provides the basis for the perceptual distinction between voiced and voiceless consonants. The present results show a lateralized processing of acoustic elements of syllables. First, processing of voiced and voiceless syllables is distinct in the left, but not in the right HG and PT. Second, only the evoked potentials in the left HG, and to a lesser extent in PT, reflect a sequential processing of the different components of the syllables. Third, we show that this acoustic temporal processing is not limited to speech sounds but applies also to non-verbal sounds mimicking the temporal structure of the syllable. Fourth, there was no difference between responses to voiced and voiceless syllables in either left or right areas 22. Our data suggest that a single mechanism in the auditory cortex, involved in general (not only speech-specific) temporal processing, may underlie the further processing of verbal (and non-verbal) stimuli. This coding, bilaterally localized in auditory cortex in animals, takes place specifically in the left HG in man. A defect of this mechanism could account for hearing discrimination impairments associated with language disorders.     

Cortical differentiation of speech and nonspeech sounds at 100 ms: implications for dyslexia

Neurophysiological measures indicate cortical sensitivity to speech sounds by 150 ms after stimulus onset. In this time window dyslexic subjects start to show abnormal cortical processing. We investigated whether phonetic analysis is reflected in the robust auditory cortical activation at approximately 100 ms (N100m), and whether dyslexic subjects show abnormal N100m responses to speech or nonspeech sounds. We used magnetoencephalography to record auditory responses of 10 normally reading and 10 dyslexic adults. The speech stimuli were synthetic Finnish speech sounds (/a/, /u/, /pa/, /ka/). The nonspeech stimuli were complex nonspeech sounds and simple sine wave tones, composed of the F1+F2+F3 and F2 formant frequencies of the speech sounds, respectively. All sounds evoked a prominent N100m response in the bilateral auditory cortices. The N100m activation was stronger to speech than nonspeech sounds in the left but not in the right auditory cortex, in both subject groups. The leftward shift of hemispheric balance for speech sounds is likely to reflect analysis at the phonetic level. In dyslexic subjects the overall interhemispheric amplitude balance and timing were altered for all sound types alike. Dyslexic individuals thus seem to have an unusual cortical organization of general auditory processing in the time window of speech-sensitive analysis.     

Distributed auditory cortical representations are modified when non-musicians are trained at pitch discrimination with 40 Hz amplitude modulated tones

Several functional brain attributes reflecting neocortical activity have been found to be enhanced in musicians compared to non-musicians. Included are the N1m evoked magnetic field, P2 and right-hemispheric N1c auditory evoked potentials, and the source waveform of the magnetically recorded 40 Hz auditory steady state response (SSR). We investigated whether these functional brain attributes measured by EEG are sensitive to neuroplastic remodeling in non-musician subjects. Adult non-musicians were trained for 15 sessions to discriminate small changes in the carrier frequency of 40 Hz amplitude modulated pure tones. P2 and N1c auditory evoked potentials were separated from the SSR by signal processing and found to localize to spatially differentiable sources in the secondary auditory cortex (A2). Training enhanced the P2 bilaterally and the N1c in the right hemisphere where auditory neurons may be specialized for processing of spectral information. The SSR localized to sources in the region of Heschl's gyrus in primary auditory cortex (A1). The amplitude of the SSR (assessed by bivariate T2 in 100 ms moving windows) was not augmented by training although the phase of the response was modified for the trained stimuli. The P2 and N1c enhancements observed here and reported previously in musicians may reflect new tunings on A2 neurons whose establishment and expression are gated by input converging from other regions of the brain. The SSR localizing to A1 was more resistant to remodeling, suggesting that its amplitude enhancement in musicians may be an intrinsic marker for musical skill or an early experience effect.     

Dynamics of oscillatory activity during auditory decision making

Perceptual decision making requires the comparison and integration of sensory evidence to generate a behavioral response. We used magnetoencephalography to investigate the temporal dynamics of decision making during an auditory task that required forced-choice decisions about whether a pair of syllables S1 and S2 differed either in their acoustic patterns or in the perceived position of their sound sources. Conditions with easy and difficult decisions were created by varying the similarity of S1 and S2. Statistical probability mapping showed enhanced gamma-band activity (GBA) over posterior parietal cortex for spatial and over left inferior frontal cortex for pattern changes (at approximately 120 to 220 ms after S2 onset). Activations were stronger for easy than difficult decisions. GBA over dorsolateral prefrontal cortex was more pronounced at approximately 280 to 430 ms for easy than difficult decisions regardless of type of change, possibly reflecting decision-relevant networks that integrate information from higher sensory areas representing the perceptual alternatives. Sensorimotor beta desynchronization as a measure of motor preparation peaked at approximately 460 ms for easy and at approximately 520 ms for difficult decisions, thus reflecting the reaction time difference between both conditions. In summary, the analysis of oscillatory activity in magnetoencephalogram served to elucidate the temporal dynamics of perceptual decision making in humans.     

Rapid distributed fronto-parieto-occipital processing stages during working memory in humans

Cortical potentials were recorded from implanted electrodes during a difficult working memory task requiring rapid storage, modification and retrieval of multiple memoranda. Synchronous event-related potentials were generated in distributed occipital, parietal, Rolandic and prefrontal sites beginning approximately 130 ms after stimulus onset and continuing for >500 ms. Coherent phase-locked, event-related oscillations supported interaction between these dorsal stream structures throughout the task period. The Rolandic structures generated early as well as sustained potentials to sensory stimuli in the absence of movement. Activation peaks and phase lags between synaptic populations suggested that perceptual processing occurred exclusively in the visual association cortex from approximately 90 to 130 ms, with its results projected to fronto-parietal areas for interpretation from approximately 130 to 280 ms. The direction of interaction then appeared to reverse from approximately 300 to 400 ms, consistent with mental arithmetic being performed by fronto-parietal areas operating upon a visual scratch pad in the dorsolateral occipital cortex. A second reversal, from approximately 420 to 600 ms, may have represented an updating of memoranda stored in fronto-parietal sites. Lateralized perisylvian oscillations suggested an articulatory loop. Anterior cingulate activity was evoked by feedback signals indicating errors. These results indicate how a fronto-centro-parietal 'central executive' might interact with an occipital visual scratch pad, perisylvian articulatory loop and limbic monitor to implement the sequential stages of a complex mental operation.     

Brain structure predicts the learning of foreign speech sounds

Previous work has shown a relationship between parietal lobe anatomy and nonnative speech sound learning. We scanned a new group of phonetic learners using structural magnetic resonance imaging and diffusion tensor imaging. Voxel-based morphometry indicated higher white matter (WM) density in left Heschl's gyrus (HG) in faster compared with slower learners, and manual segmentation of this structure confirmed that the WM volume of left HG is larger in the former compared with the latter group. This finding was replicated in a reanalysis of the original groups tested in Golestani and others (2002, Anatomical correlates of learning novel speech sounds. Neuron 35:997-1010). We also found that faster learners have a greater asymmetry (left > right) in parietal lobe volumes than slower learners and that the right insula and HG are more superiorly located in slower compared with faster learners. These results suggest that left auditory cortex WM anatomy, which likely reflects auditory processing efficiency, partly predicts individual differences in an aspect of language learning that relies on rapid temporal processing. It also appears that a global displacement of components of a right hemispheric language network, possibly reflecting individual differences in the functional anatomy and lateralization of language processing, is predictive of speech sound learning.     

Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity

Activation-dependent brain plasticity in humans on a structural level has been demonstrated in adults after 3 months of training a visio-motor skill. The exact timescale of usage-dependent structural changes, whether days, months, or years, is, however, still debated. A better understanding of the temporal parameters may help elucidate to what extent this type of cortical plasticity contributes to fast adapting cortical processes that may be relevant to learning and effects of treatments. Using voxel-based morphometry, we are able to show that repetitive transcranial magnetic stimulation delivered to the superior temporal cortex causes macroscopic cortical changes in gray matter (GM) in the auditory cortex as early as within 5 days of continuous intervention. These structural alterations are mirrored by changes in cortical evoked potentials attributed to the GM changes and demonstrate the rapid dynamics of these processes, which occur within a time range characteristic for the onset of behavioral effects induced by a variety of treatment methods for neuropsychiatric diseases. Our finding suggests that cortical plasticity on a structural level in adult humans is already detectable after 1 week, which provides support for fast adjusting neuronal systems, such as spine and synapse turnover, and contradicts slow evolving mechanisms, such as neuronal or glial cell genesis.     

Hearing lips: gamma-band activity during audiovisual speech perception

Auditory pattern changes have been shown to elicit increases in magnetoencephalographic gamma-band activity (GBA) over left inferior frontal cortex, forming part of the putative auditory ventral "what" processing stream. The present study employed a McGurk-type paradigm to assess whether GBA would be associated with subjectively perceived changes even when auditory stimuli remain unchanged. Magnetoencephalograms were recorded in 16 human subjects during audiovisual mismatch perception. Both infrequent visual (auditory /ta/ + visual /pa/) and acoustic deviants (auditory/pa/ + visual /ta/) were compared with frequent audiovisual standards (auditory /ta/ and visual /ta/). Statistical probability mapping revealed spectral amplitude increases at approximately 75 and approximately 78 Hz to visual deviants. GBA to visual deviants peaked 160 ms after auditory stimulus onset over posterior parietal cortex, at 270 ms over occipital areas and at 320 ms over left inferior frontal cortex. The latter GBA enhancement was consistent with the increase observed previously to pure acoustic mismatch, supporting a role of left inferior frontal cortex for the representation of perceived auditory pattern change. The preceding gamma-band changes over posterior areas may reflect processing of incongruent lip movements in visual motion areas and back-projections to earlier visual cortex.     

Perceptual learning on an auditory frequency discrimination task by cats: association with changes in primary auditory cortex

The aim of this study was to determine whether auditory perceptual learning is associated with changes in the frequency organization and/or neuronal response properties of primary auditory cortex (AI). Five out of six cats trained on an 8 kHz frequency discrimination task showed improvements in performance that reflected changes in discriminative capacity. Quantitative measures of the response characteristics and frequency organization of AI revealed that the frequency organization of AI in trained cats did not differ from that in controls, but there was a tendency for neurons with a CF immediately above 8 kHz to have slightly broader tuning in the trained cats than in controls, and neurons in one of these bands had significantly shorter latency. These results are in accord with recent reports that cortical topography in primary visual cortex is unchanged in animals trained on visual discrimination tasks, but are at variance with an earlier report of enlarged representations of training frequencies in AI of monkeys trained on a frequency discrimination task. It is concluded that substantial changes in perceptual discriminative capacity can occur without change in primary cortical topography and with only small changes in neuronal response characteristics.     

Age-related changes in transient and oscillatory brain responses to auditory stimulation in healthy adults 19-45 years old

The capacity of the human cerebral cortex to track fast temporal changes in auditory stimuli is related to the development of language in children and to deficits in speech perception in the elderly. Although maturation of temporal processing in children and its deterioration in the elderly has been investigated previously, little is known about naturally occurring changes in auditory temporal processing between these limits. The present study examined age-related (19-45 years) changes in 3 electrophysiological measures of auditory processing: 1) the late transient auditory evoked potentials to tone onset, 2) the auditory steady-state response (ASSR) to a 40-Hz frequency-modulated tone, and 3) the envelope following response (EFR) to sweeps of amplitude-modulated white noise from 10 to 100 Hz. With increasing age, the latency of the auditory P1-N1 complex decreased, the oscillatory (ASSR) response became larger and more stable, and the resonant peak of the EFR increased from 38 Hz at 19 years to 46 Hz at 45 years. Source analysis localized these changes to the auditory regions of the temporal lobe. These results indicate persistent adaptation of cortical auditory processes into middle adulthood. We speculate that experience-driven myelination and/or refinement of inhibitory circuits may underlie these changes.     

Training to improve hearing speech in noise: biological mechanisms

We investigated training-related improvements in listening in noise and the biological mechanisms mediating these improvements. Training-related malleability was examined using a program that incorporates cognitively based listening exercises to improve speech-in-noise perception. Before and after training, auditory brainstem responses to a speech syllable were recorded in quiet and multitalker noise from adults who ranged in their speech-in-noise perceptual ability. Controls did not undergo training but were tested at intervals equivalent to the trained subjects. Trained subjects exhibited significant improvements in speech-in-noise perception that were retained 6 months later. Subcortical responses in noise demonstrated training-related enhancements in the encoding of pitch-related cues (the fundamental frequency and the second harmonic), particularly for the time-varying portion of the syllable that is most vulnerable to perceptual disruption (the formant transition region). Subjects with the largest strength of pitch encoding at pretest showed the greatest perceptual improvement. Controls exhibited neither neurophysiological nor perceptual changes. We provide the first demonstration that short-term training can improve the neural representation of cues important for speech-in-noise perception. These results implicate and delineate biological mechanisms contributing to learning success, and they provide a conceptual advance to our understanding of the kind of training experiences that can influence sensory processing in adulthood.     

Detrimental effects of irrelevant speech on serial recall of visual items are reflected in reduced visual N1 and reduced theta activity

The term irrelevant sound effect (ISE) describes an empirically robust finding in which serial recall performance of visual items is reduced by irrelevant speech. At present little is known about its neurophysiological basis. Although some previous neuroelectric studies have concentrated on responses elicited by irrelevant background sound, whether the processing of visually presented to-be-remembered digits itself is affected by irrelevant speech has yet to be studied. An experiment (n = 20) was conducted in which serial recall performance for visually presented digits was tested during exposure to either irrelevant speech, continuous white noise or silence while measuring EEG activity. White noise was chosen as a control condition, because it constitutes auditory stimulation while leaving serial recall performance unimpaired. In addition to replicating the detrimental behavioural effect of irrelevant speech, an analogous speech-specific early decrease ( approximately 160 ms) in the visual ERP (N1) and subsequently a reduced theta response (4-6 Hz; 400-800 ms) at right prefrontal electrodes were observed. Although irrelevant sound presentation was restricted to the visual presentation phase, power spectra reveal that the weaker theta response for speech persisted in a silent retention phase before serial recall. Based on such data we propose re-evaluating the role attention plays in explaining the ISE.     

The neural basis of visual skill learning: an fMRI study of mirror reading

The learning of perceptual skills is thought to rely upon multiple regions in the cerebral cortex, but imaging studies have not yet provided evidence about the changes in neural activity that accompany visual skill learning. Functional magnetic resonance imaging (fMRI) was used to examine changes in activation of posterior brain regions associated with the acquisition of mirror-reading skill for novel and practiced stimuli. Multiple regions in the occipital lobe, inferior temporal cortex, superior parietal cortex and cerebellum were involved in the reading of mirror-reversed compared to normally oriented text. For novel stimuli, skilled mirror-reading was associated with decreased activation in the right superior parietal cortex and posterior occipital regions and increased activation in the left inferior temporal lobe. These results suggest that learning to read mirror- reversed text involves a progression from visuospatial transformation to direct recognition of transformed letters. Reading practiced, relative to unpracticed, stimuli was associated with decreased activation in occipital visual cortices, inferior temporal cortex and superior parietal cortex and increased activation in occipito-parietal and lateral temporal regions. By examining skill learning and item- specific repetition priming in the same task, this study demonstrates that both of these forms of learning exhibit shifts in the set of neural structures that contribute to performance.      

Time course of top-down and bottom-up influences on syllable processing in the auditory cortex

In speech perception, extraction of meaning from complex streams of sounds is surprisingly fast and efficient. By tracking the neural time course of syllable processing with magnetoencephalography we show that this continuous construction of meaning-based representations is aided by both top-down (context-based) expectations and bottom-up (acoustic-phonetic) cues in the speech signal. Syllables elicited a sustained response at 200-600 ms (N400m) which became most similar to that evoked by words when the expectation for meaningful speech was increased by presenting the syllables among words and sentences or using sentence-initial syllables. This word-like cortical processing of meaningless syllables emerged at the build-up of the N400m response, 200-300 ms after speech onset, during the transition from perceptual to lexical-semantic analysis. These findings show that the efficiency of meaning-based analysis of speech is subserved by a cortical system finely tuned to lexically relevant acoustic-phonetic and contextual cues.     

Right parietal brain activity precedes perceptual alternation of bistable stimuli

Momentary fluctuations of baseline activity have been shown to influence responses to sensory stimulation both behaviorally and neurophysiologically. This suggests that perceptual awareness does not solely arise from physical stimulus properties. Here we studied whether the momentary state of the brain immediately before stimulus presentation indicates how a physically unique but perceptually ambiguous stimulus will be perceived. A complex Necker cube was intermittently presented and subjects indicated whether their perception changed with respect to the preceding presentation. EEG was recorded from 256 channels. The prestimulus brain-state was defined as the spatial configuration of the scalp potential map within the 50 ms before stimulus arrival, representing the sum of all momentary ongoing brain processes. Two maps were found that doubly dissociated perceptual reversals from perceptual stability. For EEG sweeps classified as either map, distributed inverse solutions were computed and statistically compared. This yielded activity confined to a region in right inferior parietal cortex that was significantly more active before a perceptual reversal. In contrast, no significant topographic differences of the evoked potentials elicited by stable vs. reversed Necker cubes were found. This indicates that prestimulus activity in right inferior parietal cortex is associated with the perceptual change.     

Dynamics of gamma-band activity induced by auditory pattern changes in humans.

Increasing evidence suggests separate auditory pattern and space processing streams. The present paper describes two magnetoencephalogram studies examining gamma-band activity to changes in auditory patterns using consonant-vowel syllables (experiment 1), animal vocalizations and artificial noises (experiment 2). Two samples of each sound type were presented to passively listening subjects in separate oddball paradigms with 80% standards and 20% deviants differing in their spectral composition. Evoked magnetic mismatch fields peaking approximately 190 ms poststimulus showed a trend for a left-hemisphere advantage for syllables, but no hemispheric differences for the other sounds. Frequency analysis and statistical probability mapping of the differences between deviants and standards revealed increased gamma-band activity above 60 Hz over left anterior temporal/ventrolateral prefrontal cortex for all three types of stimuli. This activity peaked simultaneously with the mismatch responses for animal sounds (180 ms) but was delayed for noises (260 ms) and syllables (320 ms). Our results support the hypothesized role of anterior temporal/ventral prefrontal regions in the processing of auditory pattern change. They extend earlier findings of gamma-band activity over posterior parieto-temporal cortex during auditory spatial processing that supported the putative auditory dorsal stream. Furthermore, earlier gamma-band responses to animal vocalizations may suggest faster processing of fear-relevant information.     

Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey

Electroencephalography is increasingly being used to probe the functional organization of auditory cortex. Modulation of the electroencephalographic (EEG) signal by tones was examined in primary auditory cortex (A1) of awake monkeys. EEG data were measured at 4 laminar depths defined by current source density profiles evoked by best frequency (BF) tones. Midlaminar multiunit activity was used to define the tuning characteristics of A1 sites. Presentation of BF tones increased EEG power across the range of frequencies examined (4-290 Hz), with maximal effects evident within the first 100 ms after stimulus onset. The largest relative increases in EEG power generally occurred at very high gamma frequency bands (130-210 Hz). Increases in EEG power for frequencies less than 70 Hz primarily represented changes in phase-locked activity, whereas increases at higher frequencies primarily represented changes in non-phase-locked activity. Power increases in higher gamma bands were better correlated with the A1 tonotopic organization than power increases in lower frequency bands. Results were similar across the 4 laminar depths examined. These findings highlight the value of examining high-frequency EEG components in exploring the functional organization of auditory cortex and may enhance interpretation of related studies in humans.     

The neural correlates of conscious vision

Conflicting accounts of the neurobiology of consciousness have emerged from previous imaging studies. Some studies suggest that visual consciousness relates to a distributed network of frontal and partietal regions while others point to localized activity within individual visual areas. While the two positions seem mutually exclusive, timing issues may help reconcile the two. Networks that appear unified in functional magnetic resonance imaging (fMRI) studies may reflect processes that are widely distributed in time. To help resolve this issue, we have investigated timing across a network correlating with consciousness in parallel fMRI and evoked potential (EP) studies of grating stimuli. At threshold, a stimulus is perceived on some occasions but not on others, dissociating sensory input and perception. We have found correlates of consciousness in the occipital lobe at 100 ms and in parietal, frontal, auditory and motor regions from 260 ms onwards. The broad temporal and spatial distribution of activity argues against a unified, distributed fronto-parietal correlate of consciousness. Instead, it suggests that correlates of consciousness are divided into primary and secondary network nodes, with early activity in the occipital lobe correlating with perception and later activity in downstream areas with secondary processes contingent on the outcome of earlier perceptual processing.     

Endogenous auditory spatial attention modulates obligatory sensory activity in auditory cortex

Endogenous attention is the self-directed focus of attention to a region or feature of the environment. In this study, we assess the effects of endogenous attention on temporally detailed responses to continuous and competing auditory stimuli obtained using the novel auditory evoked spread spectrum analysis (AESPA) method. There is some debate as to whether an enhancement of sensory processing is involved in endogenous attention. It has been suggested that attentional effects are not due to increased sensory activity but are due to engagement of separate temporally overlapping nonsensory attention-related activity. There are also issues with the fact that the influence of exogenous attention grabbing mechanisms may hamper studies of endogenous attention. Due to the nature of the AESPA method, the obtained responses represent activity directly related to the stimulus envelope and thus predominantly correspond to obligatory sensory processing. In addition, the continuous nature of the stimuli minimizes exogenous attentional influence. We found attentional modulations at ~136 ms (during the Nc component of the AESPA response) and localized this to auditory cortex. Although the involvement of separate nonsensory attentional centers cannot be ruled out, these findings clearly demonstrate that endogenous attention does modulate obligatory sensory activity in auditory cortex.