Functional localization of auditory cortical fields of human: Click-train stimulation
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.
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2020, NeuroImageCitation Excerpt :Using a similar approach as Maddox and Lee (2018), by cross-correlating the fundamental waveform of continuous speech with the recorded EEG signal, Forte et al. (2017) found a distinct peak at ~9 ms. This evoked activity was modulated by attention, leading the authors to suggest a mechanism of selective attention at the level of the brainstem. However, with occurrences of early auditory cortical activity measured directly at posteromedial parts of Heschl’s Gyrus ~9–10 ms at least some thalamocortical contributions are likely (Liégeois-Chauvel et al., 1991; Brugge et al., 2008). In any case also this approach could be combined with ours, which could improve the rather small effect sizes for the reported attention effect (r < 0.06).