John F. Brugge

Representation of the cochlear partition on the superior temporal plane of the macaque monkey

Abstract The distribution of best frequencies of neurons and neuron clusters was mapped on the superior temporal plane of the macaque monkey. Primary auditory cortex (A1) comprises a complete and orderly cochlear representation. It is coextensive with a cytoarchitectonic field often referred to as koniocortex. Cochlear apex (low frequency) is represented rostrolaterally within the field and cochlear base (high frequency) caudomedially. A small region of the cochlear partition is found represented in a band of auditory cortex; that is neurons with very similar best frequencies are arrayed both vertically and horizontally. Surrounding A1 4 other fields are found that on both anatomical and physiological grounds stand apart from the primary field. In two of them the data suggest the way in which they are topographically organized. In addition there appear to be auditory areas extending further rostrally on the plane and onto the lateral surface of the superior temporal gyrus.

Temporal Position of Discharges in Single Auditory Nerve Fibers within the Cycle of a Sine‐Wave Stimulus: Frequency and Intensity Effects

Period histograms, which display the distribution of spikes throughout the period of a periodic stimulus, were computed for discharges recorded from single auditory nerve fibers of the squirrel monkey when low‐frequency tones were employed. For frequencies up to about 4 kHz, where phase locking is observed, the average phase angle of the discharges was tracked as frequency was varied in small steps from low to high. To a first approximation, the cumulative shift in average phase angle is a linear function of frequency as would be observed for an ideal delay line. The slopes of these phase‐versus‐frequency lines were found to be related through a power law to the best frequencies of the fibers. Thus, it seems possible to estimate the travel time of a mechanical disturbance between the oval window and any point on the cochlear partition. A more detailed examination revealed that average phase angle is also sensitive to intensity, depending upon the relation of the stimulating frequency to the best frequency...

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.

Direct Recordings of Pitch Responses from Human Auditory Cortex

Summary Pitch is a fundamental percept with a complex relationship to the associated sound structure [1]. Pitch perception requires brain representation of both the structure of the stimulus and the pitch that is perceived. We describe direct recordings of local field potentials from human auditory cortex made while subjects perceived the transition between noise and a noise with a regular repetitive structure in the time domain at the millisecond level called regular-interval noise (RIN) [2]. RIN is perceived to have a pitch when the rate is above the lower limit of pitch [3], at approximately 30 Hz. Sustained time-locked responses are observed to be related to the temporal regularity of the stimulus, commonly emphasized as a relevant stimulus feature in models of pitch perception (e.g., [1]). Sustained oscillatory responses are also demonstrated in the high gamma range (80–120 Hz). The regularity responses occur irrespective of whether the response is associated with pitch perception. In contrast, the oscillatory responses only occur for pitch. Both responses occur in primary auditory cortex and adjacent nonprimary areas. The research suggests that two types of pitch-related activity occur in humans in early auditory cortex: time-locked neural correlates of stimulus regularity and an oscillatory response related to the pitch percept.

Intracranial Study of Speech-Elicited Activity on the Human Posterolateral Superior Temporal Gyrus

To clarify speech-elicited response patterns within auditory-responsive cortex of the posterolateral superior temporal (PLST) gyrus, time-frequency analyses of event-related band power in the high gamma frequency range (75-175 Hz) were performed on the electrocorticograms recorded from high-density subdural grid electrodes in 8 patients undergoing evaluation for medically intractable epilepsy. Stimuli were 6 stop consonant-vowel (CV) syllables that varied in their consonant place of articulation (POA) and voice onset time (VOT). Initial augmentation was maximal over several centimeters of PLST, lasted about 400 ms, and was often followed by suppression and a local outward expansion of activation. Maximal gamma power overlapped either the Nα or Pβ deflections of the average evoked potential (AEP). Correlations were observed between the relative magnitudes of gamma band responses elicited by unvoiced stop CV syllables (/pa/, /ka/, /ta/) and their corresponding voiced stop CV syllables (/ba/, /ga/, /da/), as well as by the VOT of the stimuli. VOT was also represented in the temporal patterns of the AEP. These findings, obtained in the passive awake state, indicate that PLST discriminates acoustic features associated with POA and VOT and serve as a benchmark upon which task-related speech activity can be compared.