Auditory-cortex lesions impair contralateral tone-pattern detection under informational masking.

Impaired hearing contralateral to unilateral auditory-cortex lesions is typically only observed under conditions of perceptual competition, such as dichotic presentation or speech in noise. It remains unclear, however, if the source of this effect is direct competition in frequency-specific neurons, or if enhanced processing load in more distant frequencies can also impair auditory detection. To evaluate this question, we studied a group of patients with unilateral auditory-cortex lesions (N = 14, six left-hemispheric (LH), eight right-hemispheric (RH); four females; age range 26-72 years) and a control group (N = 25; 15 females; age range 18-76 years) with a target-detection task in presence of a multi-tone masker, which can produce informational masking. The results revealed reduced sensitivity for monaural target streams presented contralateral to auditory-cortex lesions, with an approximately 10% higher error rate in the contra-lesional ear. A general, bilateral reduction of target detection was only observed in a subgroup of patients, who were classified as additionally suffering from auditory neglect. These results demonstrate that auditory-cortex lesions impair monaural, contra-lesional target detection under informational masking. The finding supports the hypothesis that neural mechanisms beyond direct competition in frequency-specific neurons can be a source of impaired hearing under perceptual competition in patients with unilateral auditory-cortex lesions.

Transient human auditory cortex activation during volitional attention shifting.

While strong activation of auditory cortex is generally found for exogenous orienting of attention, endogenous, intra-modal shifting of auditory attention has not yet been demonstrated to evoke transient activation of the auditory cortex. Here, we used fMRI to test if endogenous shifting of attention is also associated with transient activation of the auditory cortex. In contrast to previous studies, attention shifts were completely self-initiated and not cued by transient auditory or visual stimuli. Stimuli were two dichotic, continuous streams of tones, whose perceptual grouping was not ambiguous. Participants were instructed to continuously focus on one of the streams and switch between the two after a while, indicating the time and direction of each attentional shift by pressing one of two response buttons. The BOLD response around the time of the button presses revealed robust activation of the auditory cortex, along with activation of a distributed task network. To test if the transient auditory cortex activation was specifically related to auditory orienting, a self-paced motor task was added, where participants were instructed to ignore the auditory stimulation while they pressed the response buttons in alternation and at a similar pace. Results showed that attentional orienting produced stronger activity in auditory cortex, but auditory cortex activation was also observed for button presses without focused attention to the auditory stimulus. The response related to attention shifting was stronger contralateral to the side where attention was shifted to. Contralateral-dominant activation was also observed in dorsal parietal cortex areas, confirming previous observations for auditory attention shifting in studies that used auditory cues.

Functional magnetic resonance imaging confirms forward suppression for rapidly alternating sounds in human auditory cortex but not in the inferior colliculus.

Forward suppression at the level of the auditory cortex has been suggested to subserve auditory stream segregation. Recent results in non-streaming stimulation contexts have indicated that forward suppression can also be observed in the inferior colliculus; whether this holds for streaming-related contexts remains unclear. Here, we used cardiac-gated fMRI to examine forward suppression in the inferior colliculus (and the rest of the human auditory pathway) in response to canonical streaming stimuli (rapid tone sequences comprised of either one repetitive tone or two alternating tones). The first stimulus is typically perceived as a single stream, the second as two interleaved streams. In different experiments using either pure tones differing in frequency or bandpass-filtered noise differing in inter-aural time differences, we observed stronger auditory cortex activation in response to alternating vs. repetitive stimulation, consistent with the presence of forward suppression. In contrast, activity in the inferior colliculus and other subcortical nuclei did not significantly differ between alternating and monotonic stimuli. This finding could be explained by active amplification of forward suppression in auditory cortex, by a low rate (or absence) of cells showing forward suppression in inferior colliculus, or both.

Pure word deafness with auditory object agnosia after bilateral lesion of the superior temporal sulcus.

Based on results from functional imaging, cortex along the superior temporal sulcus (STS) has been suggested to subserve phoneme and pre-lexical speech perception. For vowel classification, both superior temporal plane (STP) and STS areas have been suggested relevant. Lesion of bilateral STS may conversely be expected to cause pure word deafness and possibly also impaired vowel classification. Here we studied a patient with bilateral STS lesions caused by ischemic strokes and relatively intact medial STPs to characterize the behavioral consequences of STS loss. The patient showed severe deficits in auditory speech perception, whereas his speech production was fluent and communication by written speech was grossly intact. Auditory-evoked fields in the STP were within normal limits on both sides, suggesting that major parts of the auditory cortex were functionally intact. Further studies showed that the patient had normal hearing thresholds and only mild disability in tests for telencephalic hearing disorder. Prominent deficits were discovered in an auditory-object classification task, where the patient performed four standard deviations below the control group. In marked contrast, performance in a vowel-classification task was intact. Auditory evoked fields showed enhanced responses for vowels compared to matched non-vowels within normal limits. Our results are consistent with the notion that cortex along STS is important for auditory speech perception, although it does not appear to be entirely speech specific. Formant analysis and single vowel classification, however, appear to be already implemented in auditory cortex on the STP.

Interaction of streaming and attention in human auditory cortex.

Serially presented tones are sometimes segregated into two perceptually distinct streams. An ongoing debate is whether this basic streaming phenomenon reflects automatic processes or requires attention focused to the stimuli. Here, we examined the influence of focused attention on streaming-related activity in human auditory cortex using magnetoencephalography (MEG). Listeners were presented with a dichotic paradigm in which left-ear stimuli consisted of canonical streaming stimuli (ABA_ or ABAA) and right-ear stimuli consisted of a classical oddball paradigm. In phase one, listeners were instructed to attend the right-ear oddball sequence and detect rare deviants. In phase two, they were instructed to attend the left ear streaming stimulus and report whether they heard one or two streams. The frequency difference (ΔF) of the sequences was set such that the smallest and largest ΔF conditions generally induced one- and two-stream percepts, respectively. Two intermediate ΔF conditions were chosen to elicit bistable percepts (i.e., either one or two streams). Attention enhanced the peak-to-peak amplitude of the P1-N1 complex, but only for ambiguous ΔF conditions, consistent with the notion that automatic mechanisms for streaming tightly interact with attention and that the latter is of particular importance for ambiguous sound sequences.

Sustained selective attention to competing amplitude-modulations in human auditory cortex.

Auditory selective attention plays an essential role for identifying sounds of interest in a scene, but the neural underpinnings are still incompletely understood. Recent findings demonstrate that neural activity that is time-locked to a particular amplitude-modulation (AM) is enhanced in the auditory cortex when the modulated stream of sounds is selectively attended to under sensory competition with other streams. However, the target sounds used in the previous studies differed not only in their AM, but also in other sound features, such as carrier frequency or location. Thus, it remains uncertain whether the observed enhancements reflect AM-selective attention. The present study aims at dissociating the effect of AM frequency on response enhancement in auditory cortex by using an ongoing auditory stimulus that contains two competing targets differing exclusively in their AM frequency. Electroencephalography results showed a sustained response enhancement for auditory attention compared to visual attention, but not for AM-selective attention (attended AM frequency vs. ignored AM frequency). In contrast, the response to the ignored AM frequency was enhanced, although a brief trend toward response enhancement occurred during the initial 15 s. Together with the previous findings, these observations indicate that selective enhancement of attended AMs in auditory cortex is adaptive under sustained AM-selective attention. This finding has implications for our understanding of cortical mechanisms for feature-based attentional gain control.

Functional imaging of auditory scene analysis.

Our auditory system is constantly faced with the task of decomposing the complex mixture of sound arriving at the ears into perceptually independent streams constituting accurate representations of individual sound sources. This decomposition, termed auditory scene analysis, is critical for both survival and communication, and is thought to underlie both speech and music perception. The neural underpinnings of auditory scene analysis have been studied utilizing invasive experiments with animal models as well as non-invasive (MEG, EEG, and fMRI) and invasive (intracranial EEG) studies conducted with human listeners. The present article reviews human neurophysiological research investigating the neural basis of auditory scene analysis, with emphasis on two classical paradigms termed streaming and informational masking. Other paradigms - such as the continuity illusion, mistuned harmonics, and multi-speaker environments - are briefly addressed thereafter. We conclude by discussing the emerging evidence for the role of auditory cortex in remapping incoming acoustic signals into a perceptual representation of auditory streams, which are then available for selective attention and further conscious processing. This article is part of a Special Issue entitled Human Auditory Neuroimaging.

Role of pattern, regularity, and silent intervals in auditory stream segregation based on inter-aural time differences.

Tone triplets separated by a pause (ABA_) are a popular tone-repetition pattern to study auditory stream segregation. Such triplets produce a galloping rhythm when integrated, but isochronous rhythms when segregated. Other patterns lacking a pause may produce less-prominent rhythmic differences but stronger streaming. Here, we evaluated whether this difference is readily explained by the presence of the pause and potentially associated with the reduction of adaptation, or whether there is contribution of tone pattern per se. Sequences with repetitive ABA_ and ABAA patterns were presented in magnetoencephalography. A and B tones were separated by differences in inter-aural time differences (ΔITD). Results showed that the stronger streaming of ABAA was associated with a more prominent release from the adaptation of the P(1)m in auditory cortex. We further compared behavioral streaming responses for patterns with and without pauses, and varied the position of the pause and pattern regularity. Results showed a major effect of the pauses' presence, but no prominent effects of tone pattern or pattern regularity. These results make a case for the existence of an early, primitive streaming mechanism that does not require an analysis of the tone pattern at later stages suggested by predictive-coding models of auditory streaming. The results are better explained by the simpler population-separation model and stress the previously observed role of neural adaptation for streaming perception.

Sustained BOLD and theta activity in auditory cortex are related to slow stimulus fluctuations rather than to pitch.

Human functional MRI (fMRI) and magnetoencephalography (MEG) studies indicate a pitch-specific area in lateral Heschl's gyrus. Single-cell recordings in monkey suggest that sustained-firing, pitch-specific neurons are located lateral to primary auditory cortex. We reevaluated whether pitch strength contrasts reveal sustained pitch-specific responses in human auditory cortex. Sustained BOLD activity in auditory cortex was found for iterated rippled noise (vs. noise or silence) but not for regular click trains (vs. jittered click trains or silence). In contrast, iterated rippled noise and click trains produced similar pitch responses in MEG. Subsequently performed time-frequency analysis of the MEG data suggested that the dissociation of cortical BOLD activity between iterated rippled noise and click trains is related to theta band activity. It appears that both sustained BOLD and theta activity are associated with slow non-pitch-specific stimulus fluctuations. BOLD activity in the inferior colliculus was sustained for both stimulus types and varied neither with pitch strength nor with the presence of slow stimulus fluctuations. These results suggest that BOLD activity in auditory cortex is much more sensitive to slow stimulus fluctuations than to constant pitch, compromising the accessibility of the latter. In contrast, pitch-related activity in MEG can easily be separated from theta band activity related to slow stimulus fluctuations.

Correlates of perceptual awareness in human primary auditory cortex revealed by an informational masking experiment.

The presence of an auditory event may remain undetected in crowded environments, even when it is well above the sensory threshold. This effect, commonly known as informational masking, allows for isolating neural activity related to perceptual awareness, by comparing repetitions of the same physical stimulus where the target is either detected or not. Evidence from magnetoencephalography (MEG) suggests that auditory-cortex activity in the latency range 50-250 ms is closely coupled with perceptual awareness. Here, BOLD fMRI and MEG were combined to investigate at which stage in the auditory cortex neural correlates of conscious auditory perception can be observed. Participants were asked to indicate the perception of a regularly repeating target tone, embedded within a random multi-tone masking background. Results revealed widespread activation within the auditory cortex for detected target tones, which was delayed but otherwise similar to the activation of an unmasked control stimulus. The contrast of detected versus undetected targets revealed activity confined to medial Heschl's gyrus, where the primary auditory cortex is located. These results suggest that activity related to conscious perception involves the primary auditory cortex and is not restricted to activity in secondary areas.

Comparison of auditory deficits associated with neglect and auditory cortex lesions.

In contrast to lesions of the visual and somatosensory cortex, lesions of the auditory cortex are not associated with self-evident contralesional deficits. Only when two or more stimuli are presented simultaneously to the left and right, contralesional extinction has been observed after unilateral lesions of the auditory cortex. Because auditory extinction is also considered a sign of neglect, clinical separation of auditory neglect from deficits caused by lesions of the auditory cortex is challenging. Here, we directly compared a number of tests previously used for either auditory-cortex lesions or neglect in 29 controls and 27 patients suffering from unilateral auditory-cortex lesions, neglect, or both. The results showed that a dichotic-speech test revealed similar amounts of extinction for both auditory cortex lesions and neglect. Similar results were obtained for words lateralized by inter-aural time differences. Consistent extinction after auditory cortex lesions was also observed in a dichotic detection task. Neglect patients showed more general problems with target detection but no consistent extinction in the dichotic detection task. In contrast, auditory lateralization perception was biased toward the right in neglect but showed considerably less disruption by auditory cortex lesions. Lateralization of auditory-evoked magnetic fields in auditory cortex was highly correlated with extinction in the dichotic target-detection task. Moreover, activity in the right primary auditory cortex was somewhat reduced in neglect patients. The results confirm that auditory extinction is observed with lesions of the auditory cortex and auditory neglect. A distinction can nevertheless be made with dichotic target-detection tasks, auditory-lateralization perception, and magnetoencephalography.

Sustained responses for pitch and vowels map to similar sites in human auditory cortex.

Several studies have shown enhancement of auditory evoked sustained responses for periodic over non-periodic sounds and for vowels over non-vowels. Here, we directly compared pitch and vowels using synthesized speech with a "damped" amplitude modulation. These stimuli were parametrically varied to yield four classes of matched stimuli: (1) periodic vowels (2) non-periodic vowels, (3) periodic non-vowels, and (4) non-periodic non-vowels. 12 listeners were studied with combined MEG and EEG. Sustained responses were reliably enhanced for vowels and periodicity. Dipole source analysis revealed that a vowel contrast (vowel-non-vowel) and the periodicity-pitch contrast (periodic-non-periodic) mapped to the same site in antero-lateral Heschl's gyrus. In contrast, the non-periodic, non-vowel condition mapped to a more medial and posterior site. The sustained enhancement for vowels was significantly more prominent when the vowel identity was varied, compared to a condition where only one vowel was repeated, indicating selective adaptation of the response. These results render it unlikely that there are spatially distinct fields for vowel and pitch processing in the auditory cortex. However, the common processing of vowels and pitch raises the possibility that there is an early speech-specific field in Heschl's gyrus.

Transient bold activity locked to perceptual reversals of auditory streaming in human auditory cortex and inferior colliculus.

Our auditory system separates and tracks temporally interleaved sound sources by organizing them into distinct auditory streams. This streaming phenomenon is partly determined by physical stimulus properties but additionally depends on the internal state of the listener. As a consequence, streaming perception is often bistable and reversals between one- and two-stream percepts may occur spontaneously or be induced by a change of the stimulus. Here, we used functional MRI to investigate perceptual reversals in streaming based on interaural time differences (ITD) that produce a lateralized stimulus perception. Listeners were continuously presented with two interleaved streams, which slowly moved apart and together again. This paradigm produced longer intervals between reversals than stationary bistable stimuli but preserved temporal independence between perceptual reversals and physical stimulus transitions. Results showed prominent transient activity synchronized with the perceptual reversals in and around the auditory cortex. Sustained activity in the auditory cortex was observed during intervals where the ΔITD could potentially produce streaming, similar to previous studies. A localizer-based analysis additionally revealed transient activity time locked to perceptual reversals in the inferior colliculus. These data suggest that neural activity associated with streaming reversals is not limited to the thalamo-cortical system but involves early binaural processing in the auditory midbrain, already.

Potential fMRI correlates of 40-Hz phase locking in primary auditory cortex, thalamus and midbrain.

MEG and BOLD fMRI are both related to post-synaptic activity, but not all components of the MEG appear to be equally reflected by the BOLD response. To evaluate potential BOLD correlates of the auditory 40-Hz steady-state response (SSR), 40-Hz amplitude-modulated (AM) tones and pure-tones with 1000-Hz tone frequency and 32-s tone duration were presented to 12 listeners in fMRI and MEG. The SSR evoked by AM-tones is readily separated from the onset, offset and sustained fields in MEG by a high-pass filter. For fMRI, a contrast of AM- versus pure-tones was used to estimate activity related more specifically to the 40-Hz SSR, but excluding other activity that is evoked by AM and pure-tones alike. This contrast showed sustained BOLD activation confined to the medial part of Heschl's gyrus, the location of the primary auditory cortex, as well as activity in the medial geniculate body (MGB) and the inferior colliculus (IC). Transient BOLD onset and offset responses were prominent throughout the auditory cortex. In contrast, sustained BOLD activity for pure-tones was weak and did not match well with the time course of the sustained field, suggesting that there is no reliable BOLD correlate of the sustained field in MEG. The sustained BOLD activity in primary auditory cortex is therefore more likely linked to the phase-locked SSR. Enhanced BOLD for AM compared to pure-tones in the IC and MGB may similarly be related to phase locking.

Functional dissociation of transient and sustained fMRI BOLD components in human auditory cortex revealed with a streaming paradigm based on interaural time differences.

A number of physiological studies suggest that feature-selective adaptation is relevant to the pre-processing for auditory streaming, the perceptual separation of overlapping sound sources. Most of these studies are focused on spectral differences between streams, which are considered most important for streaming. However, spatial cues also support streaming, alone or in combination with spectral cues, but physiological studies of spatial cues for streaming remain scarce. Here, we investigate whether the tuning of selective adaptation for interaural time differences (ITD) coincides with the range where streaming perception is observed. FMRI activation that has been shown to adapt depending on the repetition rate was studied with a streaming paradigm where two tones were differently lateralized by ITD. Listeners were presented with five different ΔITD conditions (62.5, 125, 187.5, 343.75, or 687.5 µs) out of an active baseline with no ΔITD during fMRI. The results showed reduced adaptation for conditions with ΔITD ≥ 125 µs, reflected by enhanced sustained BOLD activity. The percentage of streaming perception for these stimuli increased from approximately 20% for ΔITD = 62.5 µs to > 60% for ΔITD = 125 µs. No further sustained BOLD enhancement was observed when the ΔITD was increased beyond ΔITD = 125 µs, whereas the streaming probability continued to increase up to 90% for ΔITD = 687.5 µs. Conversely, the transient BOLD response, at the transition from baseline to ΔITD blocks, increased most prominently as ΔITD was increased from 187.5 to 343.75 µs. These results demonstrate a clear dissociation of transient and sustained components of the BOLD activity in auditory cortex.

A sustained deviance response evoked by the auditory oddball paradigm.

OBJECTIVE: Previous studies have suggested that the MMN(m) is related to selective adaptation of the N(1m). Since selective adaptation has also been reported for the sustained field, we hypothesized a second deviance response in addition to the MMN(m). The present study evaluated the existence of this wave. METHODS: Magnetoencephalography was used to record deviance responses for pure tones of 1000 and 1050Hz. Tone duration was 50, 150, or 600ms in separate sets. Our hypothesis was that a sustained deviance response would increase with tone duration. RESULTS: The data revealed a sustained deviance response with a similar source configuration as the main MMN(m), but a distinct time course. The sustained deviance response increased with the tone duration, but less than the standard sustained field. Moreover, the sustained deviance response was already present for short (50ms) tones. CONCLUSIONS: The MMN(m) is followed by a sustained deviance response in the oddball paradigm. While some characteristics of the response coincide with the sustained field, its growth with tone duration differs. The response could possibly be related to automatic orienting of attention, but further studies are required to explore its functional role. SIGNIFICANCE: The sustained deviance response is a separate component--distinct from the MMN(m) and P3--that needs to be considered in the evaluation of data obtained with the auditory oddball paradigm.

Rate perception and the auditory 40-Hz steady-state fields evoked by two-tone sequences.

The rate perception of tone sequences reflects the physical repetition rate for identical sound elements. More complex sequences are perceived at the physical rate or at lower rates, depending on perceptual organization. Here, we used magnetoencephalography and psychophysical studies to evaluate the possible relationship between rate perception of such rapid, 40-Hz tone trains and the 40-Hz steady-state response (SSR) in human primary auditory cortex. In Experiment 1, the 40-Hz SSR evoked by monotone sequences of 1000 and 600 Hz were compared to the response evoked by alternating-tone sequences of the same frequencies. The results showed that the 40-Hz SSR for the alternating-tones was attenuated compared to the monotones. In Experiment 2, frequency differences across a range of 25-300 Hz were studied. Compared to a 1000-Hz monotone sequence, the 40-Hz SSR was reduced. Amplitude reduction was most prominent for frequency differences of 200 Hz and more, which were generally perceived with half-the-physical rate. We discuss possible physiological mechanisms of this finding and its relationship to perception.

The pulse-train auditory aftereffect and the perception of rapid amplitude modulations.

Prolonged listening to a pulse train with repetition rates around 100 Hz induces a striking aftereffect, whereby subsequently presented sounds are heard with an unusually "metallic" timbre [Rosenblith et al., Science 106, 333-335 (1947)]. The mechanisms responsible for this auditory aftereffect are currently unknown. Whether the aftereffect is related to an alteration of the perception of temporal envelope fluctuations was evaluated. Detection thresholds for sinusoidal amplitude modulation (AM) imposed onto noise-burst carriers were measured for different AM frequencies (50-500 Hz), following the continuous presentation of a periodic pulse train, a temporally jittered pulse train, or an unmodulated noise. AM detection thresholds for AM frequencies of 100 Hz and above were significantly elevated compared to thresholds in quiet, following the presentation of the pulse-train inducers, and both induced a subjective auditory aftereffect. Unmodulated noise, which produced no audible aftereffect, left AM detection thresholds unchanged. Additional experiments revealed that, like the Rosenblith et al. aftereffect, the effect on AM thresholds does not transfer across ears, is not eliminated by protracted training, and can last several tens of seconds. The results suggest that the Rosenblith et al. aftereffect is related to a temporary alteration in the perception of fast temporal envelope fluctuations in sounds.

Representation of auditory-filter phase characteristics in the cortex of human listeners.

Harmonic tone complexes with component phases, adjusted using a variant of a method proposed by Schroeder, can produce pure-tone masked thresholds differing by >20 dB. This phenomenon has been qualitatively explained by the phase characteristics of the auditory filters on the basilar membrane, which differently affect the flat envelopes of the Schroeder-phase maskers. We examined the influence of auditory-filter phase characteristics on the neural representation in the auditory cortex by investigating cortical auditory evoked fields (AEFs). We found that the P1m component exhibited larger amplitudes when a long-duration tone was presented in a repeating linearly downward sweeping (Schroeder positive, or m(+)) masker than in a repeating linearly upward sweeping (Schroeder negative, or m(-)) masker. We also examined the neural representation of short-duration tone pulses presented at different temporal positions within a single period of three maskers differing in their component phases (m(+), m(-), and sine phase m(0)). The P1m amplitude varied with the position of the tone pulse in the masker and depended strongly on the masker waveform. The neuromagnetic results in all cases were consistent with the perceptual data obtained with the same stimuli and with results from simulations of neural activity at the output of cochlear preprocessing. These findings demonstrate that phase effects in peripheral auditory processing are accurately reflected up to the level of the auditory cortex.

Human cortical activity during streaming without spectral cues suggests a general neural substrate for auditory stream segregation.

The brain continuously disentangles competing sounds, such as two people speaking, and assigns them to distinct streams. Neural mechanisms have been proposed for streaming based on gross spectral differences between sounds, but not for streaming based on other nonspectral features. Here, human listeners were presented with sequences of harmonic complex tones that had identical spectral envelopes, and unresolved spectral fine structure, but one of two fundamental frequencies (f0) and pitches. As the f0 difference between tones increased, listeners perceived the tones as being segregated into two streams (one stream for each f0) and cortical activity measured with functional magnetic resonance imaging and magnetoencephalography increased. This trend was seen in primary cortex of Heschl's gyrus and in surrounding nonprimary areas. The results strongly resemble those for pure tones. Both the present and pure tone results may reflect neuronal forward suppression that diminishes as one or more features of successive sounds become increasingly different. We hypothesize that feature-specific forward suppression subserves streaming based on diverse perceptual cues and results in explicit neural representations for auditory streams within auditory cortex.