Richard A. Reale

Auditory cortex on the human posterior superior temporal gyrus

The human superior temporal cortex plays a critical role in hearing, speech, and language, yet its functional organization is poorly understood. Evoked potentials (EPs) to auditory click‐train stimulation presented binaurally were recorded chronically from penetrating electrodes implanted in Heschls gyrus (HG), from pial‐surface electrodes placed on the lateral superior temporal gyrus (STG), or from both simultaneously, in awake humans undergoing surgery for medically intractable epilepsy. The distribution of averaged EPs was restricted to a relatively small area on the lateral surface of the posterior STG. In several cases, there were multiple foci of high amplitude EPs lying along this acoustically active portion of STG. EPs recorded simultaneously from HG and STG differed in their sensitivities to general anesthesia and to changes in rate of stimulus presentation. Results indicate that the acoustically active region on the STG is a separate auditory area, functionally distinct from the HG auditory field(s). We refer to this acoustically sensitive area of the STG as the posterior lateral superior temporal area (PLST). Electrical stimulation of HG resulted in short‐latency EPs in an area that overlaps PLST, indicating that PLST receives a corticocortical input, either directly or indirectly, from HG. These physiological findings are in accord with anatomic evidence in humans and in nonhuman primates that the superior temporal cortex contains multiple interconnected auditory areas. J. Comp. Neurol. 416:79–92, 2000.

The Structure of Spatial Receptive Fields of Neurons in Primary Auditory Cortex of the Cat

Transient broad-band stimuli that mimic in their spectrum and time waveform sounds arriving from a speaker in free space were delivered to the tympanic membranes of barbiturized cats via sealed and calibrated earphones. The full array of such signals constitutes a virtual acoustic space (VAS). The extracellular response to a single stimulus at each VAS direction, consisting of one or a few precisely time-locked spikes, was recorded from neurons in primary auditory cortex. Effective sound directions form a virtual space receptive field (VSRF). Near threshold, most VSRFs were confined to one quadrant of acoustic space and were located on or near the acoustic axis. Generally, VSRFs expanded monotonically with increases in stimulus intensity, with some occupying essentially all of the acoustic space. The VSRF was not homogeneous with respect to spike timing or firing strength. Typically, onset latency varied by as much as 4–5 msec across the VSRF. A substantial proportion of recorded cells exhibited a gradient of first-spike latency within the VSRF. Shortest latencies occupied a core of the VSRF, on or near the acoustic axis, with longer latency being represented progressively at directions more distant from the core. Remaining cells had VSRFs that exhibited no such gradient. The distribution of firing probability was mapped in those experiments in which multiple trials were carried out at each direction. For some cells there was a positive correlation between latency and firing probability.

Temporal envelope of time-compressed speech represented in the human auditory cortex.

Speech comprehension relies on temporal cues contained in the speech envelope, and the auditory cortex has been implicated as playing a critical role in encoding this temporal information. We investigated auditory cortical responses to speech stimuli in subjects undergoing invasive electrophysiological monitoring for pharmacologically refractory epilepsy. Recordings were made from multicontact electrodes implanted in Heschls gyrus (HG). Speech sentences, time compressed from 0.75 to 0.20 of natural speaking rate, elicited average evoked potentials (AEPs) and increases in event-related band power (ERBP) of cortical high-frequency (70–250 Hz) activity. Cortex of posteromedial HG, the presumed core of human auditory cortex, represented the envelope of speech stimuli in the AEP and ERBP. Envelope following in ERBP, but not in AEP, was evident in both language-dominant and -nondominant hemispheres for relatively high degrees of compression where speech was not comprehensible. Compared to posteromedial HG, responses from anterolateral HG—an auditory belt field—exhibited longer latencies, lower amplitudes, and little or no time locking to the speech envelope. The ability of the core auditory cortex to follow the temporal speech envelope over a wide range of speaking rates leads us to conclude that such capacity in itself is not a limiting factor for speech comprehension.

Coding of Repetitive Transients by Auditory Cortex on Heschl's Gyrus

The capacity of auditory cortex on Heschls gyrus (HG) to encode repetitive transients was studied in human patients undergoing surgical evaluation for medically intractable epilepsy. Multicontact depth electrodes were chronically implanted in gray matter of HG. Bilaterally presented stimuli were click trains varying in rate from 4 to 200 Hz. Averaged evoked potentials (AEPs) and event-related band power (ERBP), computed from responses at each of 14 recording sites, identified two auditory fields. A core field, which occupies posteromedial HG, was characterized by a robust polyphasic AEP on which could be superimposed a frequency following response (FFR). The FFR was prominent at click rates below approximately 50 Hz, decreased rapidly as click rate was increased, but could reliably be detected at click rates as high as 200 Hz. These data are strikingly similar to those obtained by others in the monkey under essentially the same stimulus conditions, indicating that mechanisms underlying temporal processing in the auditory core may be highly conserved across primate species. ERBP, which reflects increases or decreases of both phase-locked and non-phase-locked power within given frequency bands, showed stimulus-related increases in gamma band frequencies as high as 250 Hz. The AEPs recorded in a belt field anterolateral to the core were typically of low amplitude, showing little or no evidence of short-latency waves or an FFR, even at the lowest click rates used. The non-phase-locked component of the response extracted from the ERBP showed a robust, long-latency response occurring here in response to the highest click rates in the series.

Maps of auditory cortex in cats reared after unilateral cochlear ablation in the neonatal period

The responses of many neurons recorded in the high best-frequency region of primary auditory cortical field, AI, of the normal adult cat depend upon intensity differences of the sounds arriving at the two ears. These binaural interactions are exhibited early in postnatal life, well before structural maturation of the auditory pathways from the ear to the cortex is complete. The aim of the present work was to study certain aspects of the functional development of the auditory cortex in adult cats unilaterally deaf from birth. In adult animals reared with a neonatal cochlear ablation, field AI ipsilateral to the non-operated ear showed a normal tonotopic map, which was derived from single neurons and neuron clusters driven securely by best-frequency tonal stimulation in virtually every electrode penetration. The acoustic thresholds at many recording sites were as low as those obtained in AI contralateral to the non-operated ear. These findings are in marked contrast to those from control experiments on normal adult cats where only about 65% of AI neurons were excited by a sound delivered to the ipsilateral ear and where thresholds to ipsilateral ear stimulation were significantly higher than contralateral thresholds. The spatial distribution of cortical neurons based on acoustic thresholds also appeared to be different in cats unilaterally deaf from birth when compared to control cats. Closely spaced electrode penetrations in AI ipsilateral to the non-operated ear suggested that neurons were separated into low-threshold regions and high-threshold regions. There was no evidence for this type of non-random segregation in control experiments.

Auditory-visual processing represented in the human superior temporal gyrus

In natural face-to-face communication, speech perception utilizes both auditory and visual information. We described previously an acoustically responsive area on the posterior lateral surface of the superior temporal gyrus (field PLST) that is distinguishable on physiological grounds from other auditory fields located within the superior temporal plane. Considering the empirical findings in humans and non-human primates of cortical locations responsive to heard sounds and/or seen sound-sources, we reasoned that area PLST would also contain neural signals reflecting audiovisual speech interactions. To test this hypothesis, event related potentials (ERPs) were recorded from area PLST using chronically implanted multi-contact subdural surface-recording electrodes in patient-subjects undergoing diagnosis and treatment of medically intractable epilepsy, and cortical ERP maps were acquired during five contrasting auditory, visual and bimodal speech conditions. Stimulus conditions included consonant-vowel (CV) syllable sounds alone, silent seen speech or CV sounds paired with a female face articulating matched or mismatched syllables. Data were analyzed using a MANOVA framework, with the results from planned comparisons used to construct cortical significance maps. Our findings indicate that evoked responses recorded from area PLST to auditory speech stimuli are influenced significantly by the addition of visual images of the moving lower face and lips, either articulating the audible syllable or carrying out a meaningless (gurning) motion. The area of cortex exhibiting this audiovisual influence was demonstrably greater in the speech-dominant hemisphere.

Functional localization of auditory cortical fields of human: Click-train stimulation

Averaged auditory evoked potentials (AEPs) to bilaterally presented 100 Hz click trains were recorded from multiple sites simultaneously within Heschls gyrus (HG) and on the posterolateral surface of the superior temporal gyrus (STG) in epilepsy-surgery patients. Three auditory fields were identified based on AEP waveforms and their distribution. Primary (core) auditory cortex was localized to posteromedial HG. Here the AEP was characterized by a robust polyphasic low-frequency field potential having a short onset latency and on which was superimposed a smaller frequency-following response to the click train. Core AEPs exhibited the lowest response threshold and highest response amplitude at one HG site with threshold rising and amplitude declining systematically on either side of it. The AEPs recorded anterolateral to the core, if present, were typically of low amplitude, with little or no evidence of short-latency waves or the frequency-following response that characterized core AEPs. We suggest that this area is part of a lateral auditory belt system. Robust AEPs, with waveforms demonstrably different from those of the core or lateral belt, were localized to the posterolateral surface of the STG and conform to previously described field PLST.

Sensitivity of auditory cortical neurons of kittens to monaural and binaural high frequency sound

The experiments reported here describe the abilities of young auditory cortical neurons to encode information about tone bursts having frequencies above 2.5 kHz. The studies were carried out in anesthetized kittens ranging from 8 to 44 days of age. At all ages studied, stimulation of the contralateral ear was most effective in evoking spikes. Typically the response was confined to stimulus onset. Thresholds were comparatively high and response latencies were comparatively long in the youngest kittens studied. The time course of threshold development was very similar to that of the auditory nerve and cochlear nuclei indicating that most, if not all, age related thresholds and threshold changes at the cortical level are accounted for by mechanisms operating at the level of the cochlea and auditory nerve. Response latency shortened progressively over the first month of postnatal life and while the absolute change in response latency differed considerably from that of cells in the cochlear nuclei the proportional changes were very similar. These data indicate that the comparatively long response latency and latency changes recorded at the cortex are imposed by underdeveloped central auditory processes. Response areas of kitten cortical neurons resembled those of the adult. At all ages studied, binaural interactions were robust and similar in kind to those recorded in adult cats. We conclude that cortical neurons of kittens preserve the results of interactions occurring at lower brainstem levels and that the development of the circuits of which these neurons are a part develop as a functional unit.

Coding of repetitive transients by auditory cortex on posterolateral superior temporal gyrus in humans: an intracranial electrophysiology study

Evidence regarding the functional subdivisions of human auditory cortex has been slow to converge on a definite model. In part, this reflects inadequacies of current understanding of how the cortex represents temporal information in acoustic signals. To address this, we investigated spatiotemporal properties of auditory responses in human posterolateral superior temporal (PLST) gyrus to acoustic click-train stimuli using intracranial recordings from neurosurgical patients. Subjects were patients undergoing chronic invasive monitoring for refractory epilepsy. The subjects listened passively to acoustic click-train stimuli of varying durations (160 or 1,000 ms) and rates (4-200 Hz), delivered diotically via insert earphones. Multicontact subdural grids placed over the perisylvian cortex recorded intracranial electrocorticographic responses from PLST and surrounding areas. Analyses focused on averaged evoked potentials (AEPs) and high gamma (70-150 Hz) event-related band power (ERBP). Responses to click trains featured prominent AEP waveforms and increases in ERBP. The magnitude of AEPs and ERBP typically increased with click rate. Superimposed on the AEPs were frequency-following responses (FFRs), most prominent at 50-Hz click rates but still detectable at stimulus rates up to 200 Hz. Loci with the largest high gamma responses on PLST were often different from those sites that exhibited the strongest FFRs. The data indicate that responses of non-core auditory cortex of PLST represent temporal stimulus features in multiple ways. These include an isomorphic representation of periodicity (as measured by the FFR), a representation based on increases in non-phase-locked activity (as measured by high gamma ERBP), and spatially distributed patterns of activity.

Functional connections between auditory cortical fields in humans revealed by Granger causality analysis of intra-cranial evoked potentials to sounds: Comparison of two methods

Knowledge of neural interactions amongst cortical sites is important for understanding higher brain function. We studied such interactions using Granger causality (GC) to analyze auditory event-related potentials (ERPs) recorded directly and simultaneously from two physiologically identified and functionally interconnected auditory areas of cerebral cortex in human neurosurgical patients. Two methods of GC analysis were used and the results compared. Both approaches involved adaptive autoregressive modeling but differed from each other in other ways. Results obtained by using the two methods also differed. Fewer false-positive results were obtained using the method that suppressed the ERP non-stationarity and that expressed the GC as the sum of model coefficients, which suggests that this is the more appropriate approach for analyzing ERPs recorded directly from the human cortex.