Posterior Superior Temporal Plane Research Articles

Keeping track of sound objects in space: The contribution of early-stage auditory areas

The influential dual-stream model of auditory processing stipulates that information pertaining to the meaning and to the position of a given sound object is processed in parallel along two distinct pathways, the ventral and dorsal auditory streams. Functional independence of the two processing pathways is well documented by conscious experience of patients with focal hemispheric lesions. On the other hand there is growing evidence that the meaning and the position of a sound are combined early in the processing pathway, possibly already at the level of early-stage auditory areas. Here, we investigated how early auditory areas integrate sound object meaning and space (simulated by interaural time differences) using a repetition suppression fMRI paradigm at 7 T. Subjects listen passively to environmental sounds presented in blocks of repetitions of the same sound object (same category) or different sounds objects (different categories), perceived either in the left or right space (no change within block) or shifted left-to-right or right-to-left halfway in the block (change within block). Environmental sounds activated bilaterally the superior temporal gyrus, middle temporal gyrus, inferior frontal gyrus, and right precentral cortex. Repetitions suppression effects were measured within bilateral early-stage auditory areas in the lateral portion of the Heschl's gyrus and posterior superior temporal plane. Left lateral early-stages areas showed significant effects for position and change, interactions Category x Initial Position and Category x Change in Position, while right lateral areas showed main effect of category and interaction Category x Change in Position. The combined evidence from our study and from previous studies speaks in favour of a position-linked representation of sound objects, which is independent from semantic encoding within the ventral stream and from spatial encoding within the dorsal stream. We argue for a third auditory stream, which has its origin in lateral belt areas and tracks sound objects across space.

Discrimination of voice gender in the human auditory cortex

Discerning a speaker's gender from their voice is a basic and crucial aspect of human communication. Voice pitch height, the perceptual correlate of fundamental frequency, is higher in females and provides a cue for gender discrimination. However, male and female voices are also differentiated by multiple other spectral and temporal characteristics, including mean formant frequency and spectral flux. The robust perceptual segregation of male and female voices is thought to result from processing the combination of discriminating features, which in neural terms may correspond to early sound object analysis occurring in non-primary auditory cortex. However, the specific mechanism for gender perception has been unclear. Here, using functional magnetic resonance imaging, we show that discrete sites in non-primary auditory cortex are differentially activated by male and female voices, with female voices consistently evoking greater activation in the upper bank of the superior temporal sulcus and posterior superior temporal plane. This finding was observed at the individual subject-level in all 24 subjects. The neural response was highly specific: no auditory regions were more activated by male than female voices. Further, the activation associated with female voices was 1) larger than can be accounted for by a sole effect of fundamental frequency, 2) not due to psychological attribution of female gender and 3) unaffected by listener gender. These results demonstrate that male and female voices are represented as distinct auditory objects in the human brain, with the mechanism for gender discrimination being a gender-dependent activation-level cue in non-primary auditory cortex.

Changes in auditory perceptions and cortex resulting from hearing recovery after extended congenital unilateral hearing loss

Monaural hearing induces auditory system reorganization. Imbalanced input also degrades time-intensity cues for sound localization and signal segregation for listening in noise. While there have been studies of bilateral auditory deprivation and later hearing restoration (e.g., cochlear implants), less is known about unilateral auditory deprivation and subsequent hearing improvement. We investigated effects of long-term congenital unilateral hearing loss on localization, speech understanding, and cortical organization following hearing recovery. Hearing in the congenitally affected ear of a 41 year old female improved significantly after stapedotomy and reconstruction. Pre-operative hearing threshold levels showed unilateral, mixed, moderately-severe to profound hearing loss. The contralateral ear had hearing threshold levels within normal limits. Testing was completed prior to, and 3 and 9 months after surgery. Measurements were of sound localization with intensity-roved stimuli and speech recognition in various noise conditions. We also evoked magnetic resonance signals with monaural stimulation to the unaffected ear. Activation magnitudes were determined in core, belt, and parabelt auditory cortex regions via an interrupted single event design. Hearing improvement following 40 years of congenital unilateral hearing loss resulted in substantially improved sound localization and speech recognition in noise. Auditory cortex also reorganized. Contralateral auditory cortex responses were increased after hearing recovery and the extent of activated cortex was bilateral, including a greater portion of the posterior superior temporal plane. Thus, prolonged predominant monaural stimulation did not prevent auditory system changes consequent to restored binaural hearing. Results support future research of unilateral auditory deprivation effects and plasticity, with consideration for length of deprivation, age at hearing correction and degree and type of hearing loss.

Multiple Stages of Auditory Speech Perception Reflected in Event-Related fMRI

Speech processing in auditory cortex and beyond is a remarkable yet poorly understood faculty of the listening brain. Here we show that stop consonants, as the most transient constituents of speech, are sufficient to involve speech perception circuits in the human superior temporal cortex. Left anterolateral superior temporal cortex showed a stronger response in blood oxygenation level-dependent functional magnetic resonance imaging (fMRI) to intelligible consonantal bursts compared with incomprehensible control sounds matched for spectrotemporal complexity. Simultaneously, the left posterior superior temporal plane (including planum temporale [PT]) exhibited a noncategorical responsivity to complex stimulus acoustics across all trials, showing no preference for intelligible speech sounds. Multistage hierarchical processing of speech sounds is thus revealed with fMRI, providing evidence for a role of the PT in the fundamental stages of the acoustic analysis of complex sounds, including speech.

Sounds do-able: auditory–motor transformations and the posterior temporal plane

Accumulating evidence in humans and non-human primates implicates the posterior superior temporal plane (STP) in the processing of both auditory spatial information and vocal sounds. Such evidence is difficult to reconcile with existing accounts of the primate auditory brain. We propose that the posteromedial STP generates sequenced auditory representations by matching incoming auditory information with stored templates. These sequenced auditory representations are subsequently used to constrain motor responses. We argue for a re-assessment of the much-debated dorsal auditory pathway in terms of its generic behavioral role as an auditory "do" pathway.

Somatosensory input to auditory association cortex in the macaque monkey.

We investigated the convergence of somatosensory and auditory inputs in within subregions of macaque auditory cortex. Laminar current source density and multiunit activity profiles were sampled with linear array multielectrodes during penetrations of the posterior superior temporal plane in three macaque monkeys. At each recording site, auditory responses to binaural clicks, pure tones, and band-passed noise, all presented by earphones, were compared with somatosensory responses evoked by contralateral median nerve stimulation. Subjects were awake but were not required to discriminate the stimuli. Borders between A1 and surrounding belt regions were identified by mapping best frequency and stimulus preferences and by subsequent histological analysis. Regions immediately caudomedial to A1 had robust somatosensory responses co-represented with auditory responses. In these regions, both somatosensory and auditory response profiles had "feedforward" patterns; initial excitation beginning in Lamina 4 and spreading to extragranular laminae. Auditory and somatosensory responses displayed a high degree of temporal overlap. Anatomical reconstruction indicated that the somatosensory input region includes, but may not be restricted to, the caudomedial auditory association cortex. As was earlier reported for this region, auditory frequency tuning curves were broad and band-passed noise responses were larger than pure tone responses. No somatosensory responses were observed in A1. These findings suggest a potential neural substrate for multisensory integration at an early stage of auditory cortical processing.

Localization of cerebral activity during simple singing.

Cerebral blood flow (CBF) was measured with PET during rudimentary singing of a single pitch and vowel, contrasted to passive listening to complex tones. CBF increases in cortical areas related to motor control were seen in the supplementary motor area, anterior cingulate cortex, precentral gyri, anterior insula (and the adjacent inner face of the precentral operculum) and cerebellum, replicating most previously seen during speech. Increases in auditory cortex were seen within right Heschl's gyrus, and in the posterior superior temporal plane (and the immediately overlying parietal cortex). Since cortex near right Heschl's has been linked to complex pitch perception, its asymmetric activation here may be related to analyzing the fundamental frequency of one's own voice for feedback-guided modulation.

Localization of cerebral activity during simple singing

Cerebral blood flow (CBF) was measured with PET during rudimentary singing of a single pitch and vowel, contrasted to passive listening to complex tones. CBF increases in cortical areas related to motor control were seen in the supplementary motor area, anterior cingulate cortex, precentral gyri, anterior insula (and the adjacent inner face of the precentral operculum) and cerebellum, replicating most previously seen during speech. Increases in auditory cortex were seen within right Heschl's gyrus, and in the posterior superior temporal plane (and the immediately overlying parietal cortex). Since cortex near right Heschl's has been linked to complex pitch perception, its asymmetric activation here may be related to analyzing the fundamental frequency of one's own voice for feedback-guided modulation.

High-density recording and topographic analysis of the auditory oddball event-related potential in patients with schizophrenia

Background: Prior research has shown reductions of the N1, N2, and P300 auditory event-related potential (ERP) components in schizophrenic patients. Most studies have shown a greater P300 reduction in left versus right temporal leads in schizophrenic patients. These studies were done with sparse electrode arrays, covering restricted areas of the head, thus providing an incomplete representation of the topographic field distribution. Methods: We used a 64-channel montage to acquire auditory oddball ERPs from 24 schizophrenic patients and 24 controls subjects. The N1, P2, N2, P300, and N2 difference (N2d) amplitudes and latencies were tested for group and laterality differences. Component topographies were mapped onto a three-dimensional head model to display the group differences. Results: The schizophrenic group showed reduction of the N1 component, perhaps reflecting reduced arousal or vigilance, but no N1 topographic difference. An N2d was not apparent in the schizophrenic patients, perhaps reflecting severe disruption in neural systems of stimulus categorization. In the patients, the P300 was smaller over the left temporal lobe sites than the right. Conclusions: The increased ERP spatial sampling allowed a more complete representation of the dipolar nature of the P300, which showed field contours consistent with neural sources in the posterior superior temporal plane.

Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe

Event-related potentials were recorded from 537 sites in the superior temporal plane and parietal lobe of 41 patients. Depth electrodes were implanted to localize seizure origin prior to surgical treatment. Subjects received an auditory discrimination task with target and non-target rare stimuli (“standard oddball paradigm”). In some cases, the target, distracting and frequent tones were completely balanced across blocks for pitch and volume. Variants included an analogous visual discrimination task, or auditory tasks where the rare target event was the omission of a tone, or the repetition of a tone within a series of alternating tones. In some subjects, the same auditory stimuli were delivered but the patient ignored them while reading. Three general response patterns could be distinguished on the basis of their wave forms, latencies and task correlates. First, potentials apparently related to rarity per se, as opposed to differences in sensory characteristics, or in habituation, were observed in the posterior superior temporal plane, beginning with a large positivity superimposed on early components. This positivity peaked at 150 msec after stimulus onset and inverted in sites superior to the Sylvian fissure. Subsequent components could be large, focal and/or inverting in polarity, and usually included a positivity at 230 msec and a negativity at 330 msec. All components in this area were specific to the auditory modality. Second, in the posterior cingulate and supramarginal gyri, a sharp triphasic negative-positive-negative wave form with peaks at about 210-300-400 msec was observed. This wave form was of relatively small amplitude and diffuse, and seldom inverted in polarity. It was multimodal but most prominent to auditory stimuli, appeared to remain when the stimuli were ignored, and was not apparent to repeated words and faces. Third, a broad, often monophasic, wave form peaking at about 380 msec was observed in the superior parietal lobe, similar to that which has been recorded in the hippocampus. This wave form could be of large amplitude, often highly focal, and could invert over short distances. It was equal to visual and auditory stimuli and was also evoked by repeating words and faces. The early endogenous activity in auditory cortex may embody activity that is antecedent to the other patterns in multimodal association cortex. The “triphasic” pattern may embody a diffuse non-specific orienting response that is also reflected in the scalp P3a. The later broad pattern may embody the cognitive closure that is also reflected in the scalp P3b or late positive component.

Contributions of temporal-parietal junction to the human auditory P3

The P3 component of the event-related potential (ERP) is generated in humans and other mammalian species when attention is drawn to infrequent stimuli. We assessed the role of subregions of human posterior association cortex in auditory P3 generation in groups of patients with focal cortical lesions. Auditory P3s were recorded to target (P3b) and unexpected novel stimuli (P3a) in monaural and dichotic signal detection experiments. Two groups of patients were studied with lesions of: (1) temporal-parietal junction including posterior superior temporal plane and adjacent caudal inferior parietal cortex; and (2) the lateral parietal lobe including the rostral inferior parietal lobe and portions of superior parietal lobe. Extensive lateral parietal cortex lesions had no effect on the P3. In contrast, discrete unilateral lesions centered in the posterior superior temporal plane eliminated both the auditory P3b and P3a at electrodes over the posterior scalp. The results indicate that auditory association cortex in the human temporal-parietal junction is critical for auditory P3 generation.

Attention and interference in the processing of global and local information: Effects of unilateral temporal-parietal junction lesions

The processing of hierarchical stimuli was examined in patients with lesions in the temporal-parietal junction. In separate blocks of trials, subjects were instructed to identify the letter at the local or the global level of a hierarchical stimulus. Consistent with previous findings, reaction times for controls were faster in the globally than in the locally directed condition and reaction times to the local level were longer when the letters at the two levels were diffirent (e.g. local “S”s forming a global “H”) than when they were the same (e.g. local “S”s forming a global “S”). In other words, controls exhibited interference when locally directed. Patients with lesions centered in the rostral inferior parietal lobe (IPL) showed interference effects similar to controls. In contrast, patients with lesions centered in the posterior superior temporal gyrus and adjacent caudal inferior parietal lobe (STG) showed no interference. The data suggest that the posterior superior temporal plane and adjacent caudal inferior parietal lobe plays an important role in the integration of and/or attention to local and global level information.

The effects of lesions of superior temporal gyrus and inferior parietal lobe on temporal and vertex components of the human AEP

We recorded auditory evoked potentials (AEPs) to 1 kHz tone bursts in controls and patients with unilateral lesions centered in posterior superior temporal gyrus and adjacent caudal inferior parietal lobule (STG) or in rostral inferior parietal lobule (IPL). Controls generated a vertex maximal N94 (N1b) and P200 (P2) and additional P45, N78 and N127 temporal AEP components (P45, N1a, N1c). Similar to prior reports, in controls the N1a was most prominent over the left temporal lobe and the P45 was largest over the right temporal lobe consistent with behavioral and anatomical data indicating differential organization of left and right human temporal lobe. The N1c was recorded equally from both T 3 and T 4 electrodes and was enhanced in the temporal site contralateral to the ear of stimulation. The patient groups had differenti al effects on AEPs. Unilateral STG lesions resulted in bilateral reductions of the N1b and P45 and marked unilateral reductions of the N1a and N1c over lesioned hemisphere. IPL lesions resulted in bilateral but non-significant reductions of the N1b and N1c. The scalp topography results in normal subjects combined with the effects of unilateral STG lesions provide supportive evidence that the temporal maximal components of the human AEP (P45, N1a, N1c) are generated by radially oriented neuronal dipole sources located in STG. The bilateral reduction of the N1b vertex response by unilateral STG lesions is compatible with a unilateral disruption of a vertically oriented dipole situated in the posterior superior temporal plane. The results emphasize the critical role of the superior temporal plane and lateral superior temporal gyrus in generation of human long latency AEPs.

The effects of frontal and temporal-parietal lesions on the auditory evoked potential in man

We compared the properties of long-latency auditory evoked potentials (AEPs) in patients with unilateral lesions of the dorsolateral frontal cortex (N = 10) or temporal-parietal cortex (N = 10) to those of a group of age-matched normal subjects. Extensive lesions of the frontal cortex had no effect on AEP amplitudes, scalp distributions or refractory properties. However, following frontal lesions AEPs were larger to tones presented in the ear contralateral to the lesion than they were for tones presented ipsilaterally. Following unilateral temporal-parietal lesions, the N1 component (98 msec latency) was markedly reduced in amplitude at all scalp sites, and no increase in N1 amplitude occurred with lengthening ISIs. The P2 component (200 msec), however, showed the same amplitude and refractory properties as in the normal subjects. The results underline the critical role played by the cortex of the posterior-superior temporal plane and the adjacent cortex of the parietal lobe in the production of the N1 component.