Elsevier

NeuroImage

Volume 187, 15 February 2019, Pages 184-191
NeuroImage

The spatiotemporal pattern of pure tone processing: A single-trial EEG-fMRI study

https://doi.org/10.1016/j.neuroimage.2017.11.059Get rights and content

Highlights

  • We investigated the pure tone processing stream in simultaneous EEG–fMRI.

  • Single-trial ERP amplitudes serve as a regressor for an EEG–informed fMRI analysis.

  • Our results provide a spatiotemporal cascade of pure tone processing.

Abstract

Although considerable research has been published on pure tone processing, its spatiotemporal pattern is not well understood. Specifically, the link between neural activity in the auditory pathway measured by functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) markers of pure tone processing in the P1, N1, P2, and N4 components is not well established. In this study, we used single-trial EEG-fMRI as a multi-modal fusion approach to integrate concurrently acquired EEG and fMRI data, in order to understand the spatial and temporal aspects of the pure tone processing pathway. Data were recorded from 33 subjects who were presented with stochastically alternating pure tone sequences with two different frequencies: 200 and 6400 Hz. Brain network correlated with trial-to-trial variability of the task-discriminating EEG amplitude was identified. We found that neural responses responding to pure tone perception are spatially along the auditory pathway and temporally divided into three stages: (1) the early stage (P1), wherein activation occurs in the midbrain, which constitutes a part of the low level auditory pathway; (2) the middle stage (N1, P2), wherein correlates were found in areas associated with the posterodorsal auditory pathway, including the primary auditory cortex and the motor cortex; (3) the late stage (N4), wherein correlation was found in the motor cortex. This indicates that trial-by-trial variation in neural activity in the P1, N1, P2, and N4 components reflects the sequential engagement of low- and high-level parts of the auditory pathway for pure tone processing. Our results demonstrate that during simple pure tone listening tasks, regions associated with the auditory pathway transiently correlate with trial-to-trial variability of the EEG amplitude, and they do so on a millisecond timescale with a distinct temporal ordering.

Introduction

Pure tones are typical acoustic stimuli for auditory studies. They are widely used in auditory researches like auditory oddball (Milner et al., 2014), tonotopic mapping (Strainer et al., 1997) and sound pressure researches (Neuner et al., 2014). Although pure tones are the simplest and most basic auditory stimuli, the spatiotemporal pattern of neural activity during the processing of pure tones is incompletely understood. In light of the fundamental role of pure tones in auditory studies, investigating the brain processes underlying pure tone processing is helpful to investigate the processes occurring at different stages of the auditory system and understand the processing mechanisms of brain for complicated acoustic stimuli.

Existing research methods in auditory studies can be divided into invasive methods and noninvasive methods. While invasive methods (Aitkin and Webster, 1971, Rose et al., 1963) could access the dynamic processes of pure tone processing in animal experiments, obtaining comparable data in human subjects is quite challenging. Direct intracranial recordings can only be obtained in neurosurgical patients who require the placement of electrodes as part of their clinical treatment plan (Nourski et al., 2014).

Noninvasive methods such as EEG and fMRI have limitations in their capacity to resolve cortical activity in the time and space dimensions. EEG, with millisecond temporal resolution, is often used to research dynamic neural processes. However, the source localization of EEG is essentially an ill-posed problem. On the contrary, the mm-scale space resolution of fMRI allows localization of both superficial and deep sources of activity, although, its temporal resolution is poor because of the slow nature of the blood-oxygen-level dependent (BOLD) response and the low sampling rate required for the acquisition of the whole-brain fMRI data (Walz et al., 2013).

Combining EEG and fMRI can potentially provide a more sensitive measure of neuronal activity based on the complementarity between their temporal and spatial resolutions; the origin of their sources; and the potential capability of fMRI to locate EEG generators, while avoiding the EEG inverse problem (Murta et al., 2015). The fundamental assumption of EEG-fMRI integration approach is that the signals recorded with both modalities are produced by closely interacting, or at least partly overlapping, brain structures (Neuner et al., 2014). It has been suggested that the BOLD signal is governed by local field potentials (LFP) (Murta et al., 2015, Logothetis et al., 2001), which are also regarded to be the basis of neuronal signalling assessed by EEG (Neuner et al., 2014), implying that spatiotemporal data integration can be achieved by investigating correlations between BOLD and scalp EEG. EEG is a selective measure of current source activity which raises energy metabolism, whereas the haemodynamic fMRI signal is related to energy consumption of neural populations. Assuming a linear neurovascular coupling relationship (for healthy young adults) between the hemodynamic response, the LFP and the scalp EEG, the “integration by prediction” approach models the fMRI signal as a function of the EEG convolved with a canonical hemodynamic response function (Mayhew et al., 2010). This approach has proven successful for the treatment of single-trial evoked responses to establish correlations with the BOLD response using the auditory oddball P300 (Eichele et al., 2005) and task relevant ERP components (Walz et al., 2014).

During the past several years, EEG-fMRI integration methods have been used to investigate the neural processes engaged in auditory tasks. However, most of these studies focus on the brain activities related to complex auditory tasks, such as the auditory oddball (Liebenthal et al., 2003, Milner et al., 2014), auditory effortful decision making (Mulert et al., 2008), sound pressure perception (Neuner et al., 2014), task relevant auditory perception (Walz et al., 2015, Puschmann et al., 2016) and auditory attention (Wang et al., 2016). In order to get a more precise spatio-temporal interpretation of the constituent neural processes underlying the simple form of pure tone perception, a passively pure tone listening experiment with neither a complex task nor contrasts between stimulus types (e.g., standards and deviants) needs to be done. (Mayhew et al., 2010) investigated the correlations between the N1/P2 and the BOLD signal and found the activations in the SMA and the STG during P2 in a pure tone listening task. However, it has to be considered that pure tone processing is a complicated process and taking the early and late components into consideration might yield a more comprehensive view of the brain processes underlying it.

In this paper, we used simultaneously recorded EEG and fMRI during a simple listening task to spatially and temporally investigate the pure tone processing pathway. We used the single-trial analysis methodology of Eichele et al. (2005), whereby single-trial event-related potential (ERP) amplitude variability is used to construct the BOLD fMRI univariate model. Instead of focusing on the N1/P2 (Mayhew et al., 2010), we investigated the spatiotemporal evolution for BOLD correlates of auditory ERP components spanning the entire trial. We found a pure tone processing pathway, wherein the midbrain, the primary auditory cortex, and the motor cortex were sequentially activated. Our findings reveal that for the simple pure tone listening task, the auditory pathway is transiently engaged with a distinct temporal ordering and a millisecond timescale.

Section snippets

Participants

FMRI data were collected from 33 right-handed subjects (16 male, 17 female; ages 19–36 years). All subjects had normal hearing thresholds, which were determined by a hearing test administered before scanning by a trained audiologist. Hearing thresholds were better than 20 dB HL in the range between 200 and 6400 Hz. Subjects gave informed consent under a protocol approved by the Institutional Review Board of the Southwest University and were compensated for their participation.

Stimulus presentation

Stimuli were

FMRI results

Statistical maps, showing areas with significant frequency selectivity and color-coded according to the frequency of maximum response, are displayed in Fig. 3. Areas with significant frequency selectivity were found to be confined primarily to the superior temporal plane in both the hemispheres. A prominent low-frequency area with a maximal response to frequencies at 200 (red color) can be observed centrally along the superior temporal plane. It is centered on Heschl's gyrus (HG) and extends

Discussion

Here, we used single trial EEG-fMRI in combination with standard ERP and fMRI analyses to investigate the temporal and spatial course of pure tone perception. For each time window, we constructed fMRI regressors based on trial-to-trial fluctuations of the EEG amplitude and used these to model the trial-to-trial variability of events. These regressors were combined with traditional event-related regressors to model transient and mean activations. All such regressors were convolved with a

Conclusions

In conclusion, this is the first simultaneous EEG–fMRI coupling study that has looked at the processing stream of pure tone processing, capitalizing on the high temporal resolution of ERPs and the high spatial resolution of fMRI. We found the pure tone processing stream projected from the midbrain to the primary auditory cortex and then to the motor cortex. The regions identified as sensitive to pure tone stimuli in all three sequential spatiotemporal stages are consistent with the regions

Acknowledgements

This research was supported by the National Natural Science Foundation of China (61472330).

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