The spatiotemporal pattern of pure tone processing: A single-trial EEG-fMRI study
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).
References (65)
Intracortical depth analyses of frequency-sensitive regions of human auditory cortex using 7T fMRI
NeuroImage
(2016)- et al.
Tonotopic organization in the medial geniculate body of the cat
Brain Res.
(1971) - et al.
A method for removing imaging artifact from continuous EEG recorded during functional MRI
NeuroImage
(2000) Amplitopicity of the human auditory cortex: an fMRI study
NeuroImage
(2002)Tonotopic organization of the human auditory cortex as detected by BOLD-FMRI
Hear. Res.
(1998)- et al.
Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei
Brain Res. Bull.
(2003) Short frontal lobe connections of the human brain
Cortex
(2012)- et al.
Cortical surface-based analysis: I. Segmentation and surface reconstruction
NeuroImage
(1999) Corrigendum to: “Towards single-trial analysis in cognitive brain research.”
Trends Cognitive Sci.
(2008)Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: removal of the ballistocardiogram artefact
NeuroImage
(2007)
Interstimulus interval dependence of the auditory vertex response and its magnetic counterpart: implications for their neural generation
Electroencephalogr. Clin. Neurophysiol.
Tonotopic organization of human auditory cortex
NeuroImage
Simultaneous ERP and fMRI of the auditory cortex in a passive oddball paradigm
NeuroImage
Roles of supplementary motor areas in auditory processing and auditory imagery
Trends Neurosci.
Localizing pre-attentive auditory memory-based comparison: magnetic mismatch negativity to pitch change
NeuroImage
EEG signatures of auditory activity correlate with simultaneously recorded fMRI responses in humans
NeuroImage
Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection
NeuroImage
Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making
NeuroImage
Distinct cortical pathways for music and speech revealed by hypothesis-free voxel decomposition
Neuron
Tonotopic organization of the human auditory cortex revealed by transient auditory evoked magnetic fields
Electroencephalogr. Clin. Neurophysiology
Human auditory evoked potentials. I: evaluation of components
Electroencephalogr. Clin. Neurophysiol.
Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling
Clin. Neurophysiol.
An expanded role for the dorsal auditory pathway in sensorimotor control and integration
Hear. Res.
Tonotopic mapping of human auditory cortex
Hear. Res.
Simultaneous 3-T fMRI and high-density recording of human auditory evoked potentials
NeuroImage
The neuroanatomical and functional organization of speech perception
Trends Neurosci.
Population receptive field estimates of human auditory cortex
NeuroImage
Functional anatomy of human auditory attention studied with PET
NeuroImage
Prestimulus EEG alpha oscillations modulate task-related fMRI BOLD responses to auditory stimuli
NeuroImage
Simultaneous EEG-fMRI reveals a temporal cascade of task-related and default-mode activations during a simple target detection task
NeuroImage
Attention and brain function: R. Näätänen, erlbaum, Hillsdale, NJ, 1992
Acta Psychol.
Sensory-motor transformations for speech occur bilaterally
Nature
Cited by (5)
Early maturation of sound duration processing in the infant’s brain
2023, Scientific ReportsExperimental Design and Data Analysis Strategies
2023, EEG-fMRI: Physiological Basis, Technique, and Applications, Second EditionAuditory Discrimination Elicited by Nonspeech and Speech Stimuli in Children With Congenital Hearing Loss
2022, Journal of Speech, Language, and Hearing ResearchDC shifts-fMRI: A supplement to event-related fMRI
2019, Frontiers in Computational NeuroscienceSingle-trial EEG-fMRI reveals the generation process of the mismatch negativity
2019, Frontiers in Human Neuroscience