Modulation and task effects in auditory processing measured using fMRI

Research in auditory neuroscience has largely neglected the possible effects of different listening tasks on activations of auditory cortex (AC). In the present study, we used high-resolution fMRI to compare human AC activations with sounds presented during three auditory and one visual task. In all tasks, subjects were presented with pairs of Finnish vowels, noise bursts with pitch and Gabor patches. In the vowel pairs, one vowel was always either a prototypical /i/ or /ae/ (separately defined for each subject) or a nonprototype. In different task blocks, subjects were either required to discriminate (same/different) vowel pairs, to rate vowel "goodness" (first/second sound was a better exemplar of the vowel class), to discriminate pitch changes in the noise bursts, or to discriminate Gabor orientation changes. We obtained distinctly different AC activation patterns to identical sounds presented during the four task conditions. In particular, direct comparisons between the vowel tasks revealed stronger activations during vowel discrimination in the anterior and posterior superior temporal gyrus (STG), while the vowel rating task was associated with increased activations in the inferior parietal lobule (IPL). We also found that AC areas in or near Heschl's gyrus (HG) were sensitive to the speech-specific difference between a vowel prototype and nonprototype during active listening tasks. These results show that AC activations to speech sounds are strongly dependent on the listening tasks.

Speech perception in noise is a challenging everyday task with which many listeners have difficulty. Here, we report a case in which electrical brain stimulation of implanted intracranial electrodes in the left planum temporale (PT) of a neurosurgical patient significantly and reliably improved subjective quality (up to 50%) and objective intelligibility (up to 97%) of speech in noise perception. Stimulation resulted in a selective enhancement of speech sounds compared with the background noises. The receptive fields of the PT sites whose stimulation improved speech perception were tuned to spectrally broad and rapidly changing sounds. Corticocortical evoked potential analysis revealed that the PT sites were located between the sites in Heschl's gyrus and the superior temporal gyrus. Moreover, the discriminability of speech from nonspeech sounds increased in population neural responses from Heschl's gyrus to the PT to the superior temporal gyrus sites. These findings causally implicate the PT in background noise suppression and may point to a novel potential neuroprosthetic solution to assist in the challenging task of speech perception in noise.SIGNIFICANCE STATEMENT Speech perception in noise remains a challenging task for many individuals. Here, we present a case in which the electrical brain stimulation of intracranially implanted electrodes in the planum temporale of a neurosurgical patient significantly improved both the subjective quality (up to 50%) and objective intelligibility (up to 97%) of speech perception in noise. Stimulation resulted in a selective enhancement of speech sounds compared with the background noises. Our local and network-level functional analyses placed the planum temporale sites in between the sites in the primary auditory areas in Heschl's gyrus and nonprimary auditory areas in the superior temporal gyrus. These findings causally implicate planum temporale in acoustic scene analysis and suggest potential neuroprosthetic applications to assist hearing in noise.

0112 VOLUME REDUCTION OF THE LEFT PLANUM TEMPORALE GRAY MATTER ASSOCIATED WITH LONG DURATION OF UNTREATED PSYCHOSIS

Recent studies using functional imaging and electrophysiology demonstrate that processes related to sensory integration are not restricted to higher association cortices but already occur in early sensory cortices, such as primary auditory cortex. While anatomical studies suggest the superior temporal sulcus (STS) as likely source of visual input to auditory cortex, little evidence exists to support this notion at the functional level. Here we tested this hypothesis by simultaneously recording from sites in auditory cortex and STS in alert animals stimulated with dynamic naturalistic audio–visual scenes. Using Granger causality and directed transfer functions we first quantified causal interactions at the level of field potentials, and subsequently determined those frequency bands that show effective interactions, i.e. interactions that are relevant for influencing neuronal firing at the target site. We found that effective interactions from auditory cortex to STS prevail below 20 Hz, while interactions from STS to auditory cortex prevail above 20 Hz. In addition, we found that directed interactions from STS to auditory cortex make a significant contribution to multisensory influences in auditory cortex: Sites in auditory cortex showing multisensory enhancement received stronger feed-back from STS during audio–visual than during auditory stimulation, while sites with multisensory suppression received weaker feed-back. These findings suggest that beta frequencies might be important for inter-areal coupling in the temporal lobe and demonstrate that superior temporal regions indeed provide one major source of visual influences to auditory cortex.

Interaction of the effects associated with auditory-motor integration and attention-engaging listening tasks

The ability to recognize abstract features of voice during auditory perception is an intricate feat of human audition. For the listener, this occurs in near-automatic fashion to seamlessly extract complex cues from a highly variable auditory signal. Voice perception depends on specialized regions of auditory cortex, including superior temporal gyrus (STG) and superior temporal sulcus (STS). However, the nature of voice encoding at the cortical level remains poorly understood. We leverage intracerebral recordings across human auditory cortex during presentation of voice and nonvoice acoustic stimuli to examine voice encoding at the cortical level in 8 patient-participants undergoing epilepsy surgery evaluation. We show that voice selectivity increases along the auditory hierarchy from supratemporal plane (STP) to the STG and STS. Results show accurate decoding of vocalizations from human auditory cortical activity even in the complete absence of linguistic content. These findings show an early, less-selective temporal window of neural activity in the STG and STS followed by a sustained, strongly voice-selective window. Encoding models demonstrate divergence in the encoding of acoustic features along the auditory hierarchy, wherein STG/STS responses are best explained by voice category and acoustics, as opposed to acoustic features of voice stimuli alone. This is in contrast to neural activity recorded from STP, in which responses were accounted for by acoustic features. These findings support a model of voice perception that engages categorical encoding mechanisms within STG and STS to facilitate feature extraction.

SUMMARYNeuronal oscillations are suggested to play an important role in auditory working memory (WM), but their contribution to content-specific representations has remained unclear. Here, we measure magnetoencephalography during a retro-cueing task with parametric ripple-sound stimuli, which are spectrotemporally similar to speech but resist non-auditory memory strategies. Using machine learning analyses, with rigorous between-subject cross-validation and non-parametric permutation testing, we show that memorized sound content is strongly represented in phase-synchronization patterns between subregions of auditory and frontoparietal cortices. These phase-synchronization patterns predict the memorized sound content steadily across the studied maintenance period. In addition to connectivity-based representations, there are indices of more local, “activity silent” representations in auditory cortices, where the decoding accuracy of WM content significantly increases after task-irrelevant “impulse stimuli.” Our results demonstrate that synchronization patterns across auditory sensory and association areas orchestrate neuronal coding of auditory WM content. This connectivity-based coding scheme could also extend beyond the auditory domain.

In natural environments, a sound can be heard as stable despite the presence of other occasionally louder sounds. For example, when a portion in a voice is replaced by masking noise, the interrupted voice may still appear illusorily continuous. Previous research found that continuity illusions of simple interrupted sounds, such as tones, are accompanied by weaker activity in the primary auditory cortex (PAC) during the interruption than veridical discontinuity percepts of these sounds. Here, we studied whether continuity illusions of more natural and more complex sounds also emerge from this mechanism. We used psychophysics and functional magnetic resonance imaging in humans to measure simultaneously continuity ratings and blood oxygenation level-dependent activity to vowels that were partially replaced by masking noise. Consistent with previous results on tone continuity illusions, we found listeners' reports of more salient vowel continuity illusions associated with weaker activity in auditory cortex (compared with reports of veridical discontinuity percepts of physically identical stimuli). In contrast to the reduced activity to tone continuity illusions in PAC, this reduction was localized in the right anterolateral Heschl's gyrus, a region that corresponds more to the non-PAC. Our findings suggest that the ability to hear differently complex sounds as stable during other louder sounds may be attributable to a common suppressive mechanism that operates at different levels of sound representation in auditory cortex.

We aimed to investigate morphometric correlates of auditory hallucinations in bipolar disorder (BD) by comparing cortical thickness and cortical surface area in bipolar disorder patients with (BD+) and without (BD-) a lifetime history of auditory hallucinations. Based on previous findings in schizophrenia patients, we hypothesized that the cortex would be thinner in the auditory cortex in BD+ compared to BD-. Bipolar disorder spectrum (n=157) patients and healthy controls (n=279) underwent 1.5T magnetic resonance imaging (MRI) scanning. Hypothesis-driven analyses of cortical thickness and surface area in regions of the auditory cortex (Heschl's gyrus [HG], planum temporale and superior temporal gyrus) were conducted comparing BD+ (n=49) and BD- (n=108) using linear regression models, covaried for age and sex. Furthermore, we explored vertex-wise group differences in thickness and surface area across the whole cerebral cortex. Hypothesis-driven analyses:BD+ had significantly thicker cortex in the left HG compared to BD- (B=0.128, P=.0046). The finding was not explained by duration of illness, global functioning, bipolar subtype, IQ or use of antipsychotic, antidepressant or antiepileptic medication, or by lithium. Exploratory analyses: A small region of thicker cortex in BD+ compared to BD- was seen in the left superior parietal lobule (false discovery rate <0.05). There were no significant group differences in cortical surface area. A lifetime history of auditory hallucinations in BD was associated with cortical thickness alterations in both the left HG and the superior parietal lobule. Contrary to our hypothesis, BD+ showed thicker, rather than thinner cortex compared to BD-. Replications in independent samples are needed.

Effective connectivity analysis demonstrates involvement of premotor cortex during speech perception

Primary auditory cortex is a critical stage in the human auditory pathway, a gateway between subcortical and higher-level cortical areas. Receiving the output of all subcortical processing, it sends its output on to higher-level cortex. Non-invasive physiological recordings of primary auditory cortex using electroencephalography (EEG) and magnetoencephalography (MEG), however, may not have sufficient specificity to separate responses generated in primary auditory cortex from those generated in underlying subcortical areas or neighboring cortical areas. This limitation is important for investigations of effects of top-down processing (e.g., selective-attention-based) on primary auditory cortex: higher-level areas are known to be strongly influenced by top-down processes, but subcortical areas are often assumed to perform strictly bottom-up processing. Fortunately, recent advances have made it easier to isolate the neural activity of primary auditory cortex from other areas. In this perspective, we focus on time-locked responses to stimulus features in the high gamma band (70-150 Hz) and with early cortical latency (∼40 ms), intermediate between subcortical and higher-level areas. We review recent findings from physiological studies employing either repeated simple sounds or continuous speech, obtaining either a frequency following response (FFR) or temporal response function (TRF). The potential roles of top-down processing are underscored, and comparisons with invasive intracranial EEG (iEEG) and animal model recordings are made. We argue that MEG studies employing continuous speech stimuli may offer particular benefits, in that only a few minutes of speech generates robust high gamma responses from bilateral primary auditory cortex, and without measurable interference from subcortical or higher-level areas.

Event Abstract Back to Event Causal role of auditory cortex in mediating attention to moments in time Attention is the means by which the brain selects and highlights important sensory information for further processing, ignoring or suppressing the rest. The earliest single unit studies revealed that neural activity in the first stages of cortical sensory processing is modulated by attention (Hubel et al., 1959). To date, most of what is known about the neural mechanisms underlying attention is based on correlations between neural activity and behavior. Here we establish for the first time that not only is neural activity in the auditory cortex correlated with attention, but that the auditory cortex is causally involved in mediating the behavioral advantages conferred by attention. We first developed a rodent behavioral paradigm in which we could demonstrate that attention enhanced performance on a sensory discrimination task. The task was an auditory two-alternative choice paradigm, modeled after a related visual paradigm in humans (Coull and Nobre, 1998), in which we manipulated attention to moments in time. Rats were required to detect a frequency-modulated target sound immersed in a train of pure tone distractors. Performance varied systematically with task difficulty, manipulated by the varying modulation depth of the target. Behavioral analysis showed a clear improvement in both reaction times and correct discrimination whenever the target appeared at an expected moment, compared to the same target appearing unexpectedly. These results show that attention improved performance. We next used tetrodes to record responses from single neurons in the primary auditory cortex of rats performing this task. The majority of responsive neurons showed an increase evoked response to tones immediately preceding the expected appearance of the target when compared against responses to the same tones occurring long before the expected target location. These results show that attention to moments in time modulates changes in neural activity in the auditory cortex. Finally, we assessed the effect on performance of pharmacological inactivation of the auditory cortex. We used the GABA-A receptor agonist muscimol to reversibly inactivate the auditory cortex bilaterally. Muscimol inactivation impaired performance compared with control application of saline, implying that the auditory cortex plays an important role in this task under normal conditions. Furthermore, inactivation of the auditory cortex significantly reduced the improvements in performance associated with attention. These results suggest that the auditory cortex is required to mediate the behavioral advantage conferred by attention. In summary, we have shown that: (1) attention to moments in time can lead to improved performance on a two-alternative choice auditory detection/discrimination task in rats; (2) neural activity in the primary auditory cortex is correlated with attention to moments in time; and (3) the auditory cortex plays a causal role in mediating the behavioral advantage conferred by attention.

Gender differences in hemispheric asymmetry for language functioning have been reported in the neuropsychological literature. Despite numerous reports of anatomic asymmetries in corresponding cortical regions, the possibility of gender dimorphism in the putative neuroanatomical substrate of language has not been systematically examined in vivo. We assessed asymmetry of the planum temporale (PT), a supratemporal region of auditory association cortex, in 12 normal, right-handed females and 12 age-matched right-handed males with the aid of MRI surface-rendering morphometry. Bilateral areas were also assessed for Heschl's gyrus (HG), a supratemporal region of primary auditory cortex where no asymmetry was anticipated. We found a significant interaction between gender and hemisphere for the PT, with males having significantly larger left versus right PTs. Left-right differences in PT area were not significant among females (10 of 12 males showed leftward lateralization of the PT, vs 5 of 12 females). No main effect of gender was found for total (left + right) PT area, and no asymmetries or gender effects were detected for HG. This finding of gender dimorphism in PT area is consistent with evidence for reduced asymmetry among females in the lateralization of language functions attributable to the supratemporal cortex. The implications for theories about interactions between sex hormones and the development of brain asymmetries are discussed.

Induced oscillatory activity in the auditory cortex peaks at around 40 Hz in humans. Using regional cerebral blood flow and positron emission tomography we previously confirmed frequency-selective cortical responses to 40-Hz tones in auditory primary cortices and concomitant bilateral activation of the cerebellar hemispheres. In this study, using functional magnetic resonance imaging (fMRI) we estimated the influence of 40-Hz auditory stimulation on the coupling between auditory cortex and superior temporal sulcus (STS) and Crus II, using a dynamic causal model of the interactions between medial geniculate nuclei, auditory superior temporal gyrus (STG)/STS, and the cerebellar Crus II auditory region. Specifically, we tested the hypothesis that 40-Hz-selective responses in the cerebellar Crus II auditory region could be explained by frequency-specific enabling of interactions in the auditory cortico–cerebellar–thalamic loop. Our model comparison results suggest that input from auditory STG/STS to cerebellum is enhanced selectively at gamma-band frequencies around 40 Hz.

Many studies have demonstrated significant sexual dimorphism in verbal ability. However, few studies have examined anatomical differences between the sexes that may underlie such dimorphism. To examine sex differences in the absolute and proportional volumes of the main language-associated regions of the cerebral cortex. Control neuropathological case series of consecutive autopsies from a teaching hospital. No significant age-related volume changes were identified in the sample. Two language-associated cortical regions, the superior temporal gyrus (part of the Wernicke area) and its subdivisions (planum temporale, Heschl gyrus, and anterior superior temporal gyrus) and the inferior frontal gyrus (Broca area in the dominant hemisphere), and a non-language-associated region, the frontal pole, were measured using stereological techniques in brains fixed with formaldehyde solution serially sectioned at 3-mm intervals. Volume comparisons between the sexes and between brain hemispheres were performed using 2-way analysis of variance. Studies were conducted at the University of Sydney and the Prince of Wales Medical Research Institute, Sydney, Australia. Ten males and 11 females free from neurologic or neuropathological abnormalities. The volume of the superior temporal cortex, expressed as a proportion of total cerebral volume, was significantly larger in females compared with males (17.8% increase; P = .04). This was accounted for by 1 section of the superior temporal cortex, the planum temporale, which was 29.8% larger in females (P = .04). In addition, the cortical volume fraction of the Broca area in females was 20.4% larger than in males (P = .05). In contrast, no significant differences were found in the proportional volume of the frontal pole or in regional volumes between the left and right hemispheres in either sex group. Our results suggest that females have proportionally larger Wernicke and Broca language-associated regions compared with males. These anatomical differences may correlate with superior language skills previously demonstrated in females.