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

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Abstract

Averaged auditory evoked potentials (AEPs) to bilaterally presented 100 Hz click trains were recorded from multiple sites simultaneously within Heschl’s 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.

Introduction

Human auditory cortex is composed of multiple fields distributed both on the exposed surface of the superior temporal gyrus (STG) and in areas buried within the Sylvian fissure beneath the overlying parietal cortex on the supratemporal plane. The numbers, locations and boundaries of the fields are not well known nor are homologies with cortical auditory fields of non-human primates well delineated. Cytoarchitectonic studies have consistently identified a patch of koniocortex confined to the posteromedial portion of the transverse temporal gyrus of Heschl (HG) that is also heavily myelinated and exhibits a distinct chemoarchitecture (reviewed by Hackett, 2003). Although traditionally considered the site of the primary auditory field (AI), this area is not homogeneous in its cellular architecture (Galaburda and Sanides, 1980, Morosan et al., 2001, Fullerton and Pandya, 2007) suggesting that it may represent more than one primary or ‘primary-like’ field and, thus, may better be considered a primary cortical complex or, as in monkey, an auditory core (Hackett et al., 2001). Anatomical studies have also consistently shown a belt of cortical fields on the superior temporal plane adjacent to, and distinct from, the core koniocortex. Although there is not full agreement on the number and locations of belt fields, as many as seven have been identified on histochemical grounds (Rivier and Clarke, 1997, Wallace et al., 2002). One or two auditory fields have been identified lateral to belt fields, on the posterolateral exposed surface of the STG (Wallace et al., 2002, Sweet et al., 2005).

Auditory evoked potentials (AEPs) obtained in response to a wide range of both simple and complex sound have been recorded directly from the superior temporal plane of neurosurgical patients both acutely in the operating room (Sem-Jacobsen et al., 1956, Chatrian et al., 1960, Celesia and Puletti, 1969, Celesia and Puletti, 1971, Puletti and Celesia, 1970, Celesia, 1976) or chronically through implanted multi-channel depth electrodes (Lee et al., 1984, Liegeois-Chauvel et al., 1991, Liegeois-Chauvel et al., 1994, Howard et al., 1996b, Howard et al., 2000, Steinschneider et al., 1999, Steinschneider et al., 2005, Fishman et al., 2001, Yvert et al., 2002, Yvert et al., 2005, Trebuchon-Da Fonseca et al., 2005, Bidet-Caulet et al., 2007). In cases where there was adequate anatomical localization of recording sites, these AEPs were localized to a relatively restricted area of posteromedial HG, which was taken to be the primary auditory field. Robustly-responsive, frequency-tuned and tonotopically-organized neurons and neuronal clusters were recorded in cortex of the posteromedial HG by Howard et al. (1996b), which provided direct evidence for this area being considered field AI. In comparison to posteromedial HG, waveforms recorded more anterolaterally are dominated by AEPs of relatively longer latency and lower amplitude (Celesia, 1976, Liegeois-Chauvel et al., 1991, Liegeois-Chauvel et al., 1994) signaling perhaps a second auditory field on HG adjacent to the auditory core. Additionally, AEPs recorded directly from the posterolateral STG exhibit waveforms and response sensitivity demonstrably different from that recorded on HG, and on this basis we earlier referred to the area as the posterolateral superior temporal auditory field (area PLST, Howard et al., 2000, Brugge et al., 2003, Brugge et al., 2005).

Although many questions still remain unanswered regarding homologies with auditory cortical fields of non-human primates (Hackett et al., 2001, Hackett, 2003, Sweet et al., 2005), studies of auditory cortex in monkey continue to guide research in human (see Scott, 2005). Based on cellular architecture, patterns of connections and tone-frequency maps, a dozen or more auditory or auditory-related fields have been identified in monkey and broadly grouped into four processing levels (Kaas and Hackett, 2000). A core of as many as three koniocortical fields, including AI, on the supratemporal plane is flanked by perhaps seven auditory belt fields. Belt fields project topographically upon two or more parabelt fields which, in turn, make connections with more distant cortex of the temporal, parietal and frontal lobes. A hierarchical serial/parallel processing model derived from anatomical and physiological studies of these fields posits that information about spectro-temporal features of a natural sound are preserved in core cortex and from there disseminated to belt and parabelt fields where through convergent and divergent interactions they are transformed and integrated into more complex cerebral representations (Rauschecker, 1998, Kaas and Hackett, 2000). Although there is general agreement that the auditory core koniocortex in human is homologous to that of the non-human primate, far less certain are homologies regarding belt and parabelt fields (Hackett et al., 2001, Hackett, 2003, Sweet et al., 2005, Fullerton and Pandya, 2007). Nonetheless, evidence from fMRI studies suggests that a functional hierarchy may also exist for human auditory cortex (Wessinger et al., 2001), which may be incorporated into dual-stream models of cortical processing of complex sound, including speech (Rauschecker and Tian, 2000, Griffiths et al., 2004, Hickok and Poeppel, 2004, Hickok and Poeppel, 2007). Thus, while the non-human primate model of auditory cortical processing continues to be useful in guiding human studies, it is essential to carry out studies directly in humans using a variety of complementary experimental approaches if we are to understand fully the functional organization of human auditory cortex and especially the mechanisms underlying the perception of speech and other complex sound.

Our aim is to localize and characterize physiologically the auditory cortical fields of the STG in the human. Our approach in doing so is to record directly from auditory cortex of epilepsy-surgery patients while they listen, and in some cases respond behaviorally, to a wide range of controlled sounds. In this paper we describe the results of a series of experiments in which the AEPs to a brief click train (5 clicks at 100 Hz) were recorded simultaneously through multi-contact electrodes chronically implanted within HG and on the exposed surface of the posterolateral STG. Using this stimulus we were able to distinguish one field from another based not only on the waveform of the AEP evoked by the abrupt onset of the click train but also by the synchronized, frequency-following, response (FFR) to individual clicks in the train. By mapping the distribution AEPs and the FFR, and relating these waveforms to anatomically confirmed recording locations, we have identified at least three auditory cortical fields – two on HG and a third on the posterolateral surface of the STG.

Section snippets

Materials and methods

Studies have been carried out on 25 patients undergoing evaluation to identify a seizure focus prior to surgery aimed at alleviating their medically intractable epilepsy. Research protocols were approved by the University of Iowa Human Subjects Review Board. Prior informed consent was obtained from each patient enrolled in the study. As part of the treatment plan depth electrodes were inserted into HG on the supratemporal plane while grid electrodes were implanted over perisylvian cortex of the

Results

Two auditory fields on HG and one on the posterolateral surface of the STG were distinguished based on the characteristics of the waveforms evoked by the 100 click-train stimulus. Fig. 1 illustrates activity recorded from these fields in one patient whose AEPs were obtained simultaneously from 14 micro-contacts and four macro-contacts on a HDE that traversed, within gray matter, the long axis of HG, and from 96 contacts of a grid overlaying the posterolateral STG. Recordings were made on the

Discussion

We have identified what we believe to be three auditory fields on the human STG based on the amplitude and time structure of AEP waveforms recorded in response to 100 Hz click trains. We interpret the activity recorded in posteromedial HG as arising from a primary (core) auditory field. AEPs recorded here are characterized by their relatively large amplitude, short onset latency and a FFR. The amplitude of the AEP, including the FFR, is greatest at one recording location and diminishes with

Acknowledgements

We wish to thank Carol Dizack for graphic art work, and Peter Luo and Haiming Chen for computer programming and electronic instrumentation. Charles Garell, Hans Bakken, Kirill Nourski participated in some of these experiments. This work was supported by NIH Grants DC-04290, HD-03352, MH-070497 and MO1-RR-59 (General Clinical Research Centers Program) and by the Hoover Fund and Carver Trust.

References (55)

  • J. Rademacher et al.

    Probabilistic mapping and volume measurement of human primary auditory cortex

    Neuroimage

    (2001)
  • J.P. Rauschecker

    Cortical processing of complex sounds

    Curr. Opin. Neurol.

    (1998)
  • R.A. Reale et al.

    Auditory-visual processing represented in the human superior temporal gyrus

    Neuroscience

    (2007)
  • F. Rivier et al.

    Cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas

    Neuroimage

    (1997)
  • S.K. Scott

    Auditory processing – speech, space and auditory objects

    Curr. Opin. Neurobiol.

    (2005)
  • C.W. Sem-Jacobsen et al.

    Electroencephalographic rhythms from the depths of the parietal, occipital and temporal lobes in man

    EEG Clin. Neurophysiol.

    (1956)
  • M. Steinschneider et al.

    Cellular generators of the cortical auditory evoked potential initial component

    Electroencephalogr. Clin. Neurophysiol.

    (1992)
  • A. Trebuchon-Da Fonseca et al.

    Hemispheric lateralization of voice onset time (VOT) comparison between depth and scalp EEG recordings

    Neuroimage

    (2005)
  • B. Yvert et al.

    Localization of human supratemporal auditory areas from intracerebral auditory evoked potentials using distributed source models

    Neuroimage

    (2005)
  • P. Bailey et al.

    The Isocortex of Man

    (1951)
  • A. Bidet-Caulet et al.

    Effects of selective attention on the electrophysiological representation of concurrent sounds in the human auditory cortex

    J. Neurosci.

    (2007)
  • J.R. Binder et al.

    Human temporal lobe activation by speech and nonspeech sounds

    Cereb. Cortex

    (2000)
  • Brodmann, K. 1909. Vergleichende Loakalisationslehre der Grosshirnrinde J.A. Barth,...
  • J.F. Brugge et al.

    Functional connections between auditory cortex on Heschl’s gyrus and on the lateral superior temporal gyrus in humans

    J. Neurophysiol.

    (2003)
  • J.F. Brugge et al.

    The posteriolateral superior temporal auditory field in humans. Functional organization and connectivity

  • G.G. Celesia

    Organization of auditory cortical areas in man

    Brain

    (1976)
  • G.G. Celesia et al.

    Auditory cortical areas of man

    Neurology

    (1969)
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