Wei-Tang Chang

Dynamic Oscillatory Processes Governing Cued Orienting and Allocation of Auditory Attention

In everyday listening situations, we need to constantly switch between alternative sound sources and engage attention according to cues that match our goals and expectations. The exact neuronal bases of these processes are poorly understood. We investigated oscillatory brain networks controlling auditory attention using cortically constrained fMRI-weighted magnetoencephalography/EEG source estimates. During consecutive trials, participants were instructed to shift attention based on a cue, presented in the ear where a target was likely to follow. To promote audiospatial attention effects, the targets were embedded in streams of dichotically presented standard tones. Occasionally, an unexpected novel sound occurred opposite to the cued ear to trigger involuntary orienting. According to our cortical power correlation analyses, increased frontoparietal/temporal 30–100 Hz gamma activity at 200–1400 msec after cued orienting predicted fast and accurate discrimination of subsequent targets. This sustained correlation effect, possibly reflecting voluntary engagement of attention after the initial cue-driven orienting, spread from the TPJ, anterior insula, and inferior frontal cortices to the right FEFs. Engagement of attention to one ear resulted in a significantly stronger increase of 7.5–15 Hz alpha in the ipsilateral than contralateral parieto-occipital cortices 200–600 msec after the cue onset, possibly reflecting cross-modal modulation of the dorsal visual pathway during audiospatial attention. Comparisons of cortical power patterns also revealed significant increases of sustained right medial frontal cortex theta power, right dorsolateral pFC and anterior insula/inferior frontal cortex beta power, and medial parietal cortex and posterior cingulate cortex gamma activity after cued versus novelty-triggered orienting (600–1400 msec). Our results reveal sustained oscillatory patterns associated with voluntary engagement of auditory spatial attention, with the frontoparietal and temporal gamma increases being best predictors of subsequent behavioral performance.

Whole-head rapid fMRI acquisition using echo-shifted magnetic resonance inverse imaging.

The acquisition time of BOLD contrast functional MRI (fMRI) data with whole-brain coverage typically requires a sampling rate of one volume in 1-3s. Although the volumetric sampling time of a few seconds is adequate for measuring the sluggish hemodynamic response (HDR) to neuronal activation, faster sampling of fMRI might allow for monitoring of rapid physiological fluctuations and detection of subtle neuronal activation timing information embedded in BOLD signals. Previous studies utilizing a highly accelerated volumetric MR inverse imaging (InI) technique have provided a sampling rate of one volume per 100 ms with 5mm spatial resolution. Here, we propose a novel modification of this technique, the echo-shifted InI, which allows TE to be longer than TR, to measure BOLD fMRI at an even faster sampling rate of one volume per 25 ms with whole-brain coverage. Compared with conventional EPI, echo-shifted InI provided an 80-fold speedup with similar spatial resolution and less than 2-fold temporal SNR loss. The capability of echo-shifted InI to detect HDR timing differences was tested empirically. At the group level (n=6), echo-spaced InI was able to detect statistically significant HDR timing differences of as low as 50 ms in visual stimulus presentation. At the level of individual subjects, significant differences in HDR timing were detected for 400 ms stimulus-onset differences. Our results also show that the temporal resolution of 25 ms is necessary for maintaining the temporal detecting capability at this level. With the capabilities of being able to distinguish the timing differences in the millisecond scale, echo-shifted InI could be a useful fMRI tool for obtaining temporal information at a time scale closer to that of neuronal dynamics.

K-space reconstruction of magnetic resonance inverse imaging (K-InI) of human visuomotor systems

Using simultaneous measurements from multiple channels of a radio-frequency coil array, magnetic resonance inverse imaging (InI) can achieve ultra-fast dynamic functional imaging of the human with whole-brain coverage and a good spatial resolution. Mathematically, the InI reconstruction is a generalization of parallel MRI (pMRI), which includes image space and k-space reconstructions. Because of the auto-calibration technique, the pMRI k-space reconstruction offers more robust and adaptive reconstructions compared to the image space algorithm. Here we present the k-space InI (K-InI) reconstructions to reconstruct the highly accelerated BOLD-contrast fMRI data of the human brain to achieve 100 ms temporal resolution. Simulations show that K-InI reconstructions can offer 3D image reconstructions at each time frame with reasonable spatial resolution, which cannot be obtained using the previously proposed image space minimum-norm estimates (MNE) or linear constraint minimum variance (LCMV) spatial filtering reconstructions. The InI reconstructions of in vivo BOLD-contrast fMRI data during a visuomotor task show that K-InI offer 3 to 5 fold more sensitive detection of the brain activation than MNE and a comparable detection sensitivity to the LCMV reconstructions. The group average of the high temporal resolution K-InI reconstructions of the hemodynamic response also shows a relative onset timing difference between the visual (first) and somatomotor (second) cortices by 400 ms (600 ms time-to-peak timing difference). This robust and sensitive K-InI reconstruction can be applied to dynamic MRI acquisitions using a large-n coil array to improve the spatiotemporal resolution.

Combined MEG and EEG show reliable patterns of electromagnetic brain activity during natural viewing

Naturalistic stimuli such as movies are increasingly used to engage cognitive and emotional processes during fMRI of brain hemodynamic activity. However, movies have been little utilized during magnetoencephalography (MEG) and EEG that directly measure population-level neuronal activity at a millisecond resolution. Here, subjects watched a 17-min segment from the movie Crash (Lionsgate Films, 2004) twice during simultaneous MEG/EEG recordings. Physiological noise components, including ocular and cardiac artifacts, were removed using the DRIFTER algorithm. Dynamic estimates of cortical activity were calculated using MRI-informed minimum-norm estimation. To improve the signal-to-noise ratio (SNR), principal component analyses (PCA) were employed to extract the prevailing temporal characteristics within each anatomical parcel of the Freesurfer Desikan-Killiany cortical atlas. A variety of alternative inter-subject correlation (ISC) approaches were then utilized to investigate the reliability of inter-subject synchronization during natural viewing. In the first analysis, the ISCs of the time series of each anatomical region over the full time period across all subject pairs were calculated and averaged. In the second analysis, dynamic ISC (dISC) analysis, the correlation was calculated over a sliding window of 200 ms with 3.3 ms steps. Finally, in a between-run ISC analysis, the between-run correlation was calculated over the dynamic ISCs of the two different runs after the Fisher z-transformation. Overall, the most reliable activations occurred in occipital/inferior temporal visual and superior temporal auditory cortices as well as in the posterior cingulate, precuneus, pre- and post-central gyri, and right inferior and middle frontal gyri. Significant between-run ISCs were observed in superior temporal auditory cortices and inferior temporal visual cortices. Taken together, our results show that movies can be utilized as naturalistic stimuli in MEG/EEG similarly as in fMRI studies.

Intracortical depth analyses of frequency-sensitive regions of human auditory cortex using 7T fMRI

Despite recent advances in auditory neuroscience, the exact functional organization of human auditory cortex (AC) has been difficult to investigate. Here, using reversals of tonotopic gradients as the test case, we examined whether human ACs can be more precisely mapped by avoiding signals caused by large draining vessels near the pial surface, which bias blood-oxygen level dependent (BOLD) signals away from the actual sites of neuronal activity. Using ultra-high field (7T) fMRI and cortical depth analysis techniques previously applied in visual cortices, we sampled 1mm isotropic voxels from different depths of AC during narrow-band sound stimulation with biologically relevant temporal patterns. At the group level, analyses that considered voxels from all cortical depths, but excluded those intersecting the pial surface, showed (a) the greatest statistical sensitivity in contrasts between activations to high vs. low frequency sounds and (b) the highest inter-subject consistency of phase-encoded continuous tonotopy mapping. Analyses based solely on voxels intersecting the pial surface produced the least consistent group results, even when compared to analyses based solely on voxels intersecting the white-matter surface where both signal strength and within-subject statistical power are weakest. However, no evidence was found for reduced within-subject reliability in analyses considering the pial voxels only. Our group results could, thus, reflect improved inter-subject correspondence of high and low frequency gradients after the signals from voxels near the pial surface are excluded. Using tonotopy analyses as the test case, our results demonstrate that when the major physiological and anatomical biases imparted by the vasculature are controlled, functional mapping of human ACs becomes more consistent from subject to subject than previously thought.

Lateralized parietotemporal oscillatory phase synchronization during auditory selective attention

Based on the infamous left-lateralized neglect syndrome, one might hypothesize that the dominating right parietal cortex has a bilateral representation of space, whereas the left parietal cortex represents only the contralateral right hemispace. Whether this principle applies to human auditory attention is not yet fully clear. Here, we explicitly tested the differences in cross-hemispheric functional coupling between the intraparietal sulcus (IPS) and auditory cortex (AC) using combined magnetoencephalography (MEG), EEG, and functional MRI (fMRI). Inter-regional pairwise phase consistency (PPC) was analyzed from data obtained during dichotic auditory selective attention task, where subjects were in 10-s trials cued to attend to sounds presented to one ear and to ignore sounds presented in the opposite ear. Using MEG/EEG/fMRI source modeling, parietotemporal PPC patterns were (a) mapped between all AC locations vs. IPS seeds and (b) analyzed between four anatomically defined AC regions-of-interest (ROI) vs. IPS seeds. Consistent with our hypothesis, stronger cross-hemispheric PPC was observed between the right IPS and left AC for attended right-ear sounds, as compared to PPC between the left IPS and right AC for attended left-ear sounds. In the mapping analyses, these differences emerged at 7-13Hz, i.e., at the theta to alpha frequency bands, and peaked in Heschls gyrus and lateral posterior non-primary ACs. The ROI analysis revealed similarly lateralized differences also in the beta and lower theta bands. Taken together, our results support the view that the right parietal cortex dominates auditory spatial attention.

Sparse current source estimation for MEG using loose orientation constraints

Spatially focal source estimates for magnetoencephalography (MEG) and electroencephalography (EEG) data can be obtained by imposing a minimum ℓ1‐norm constraint on the distribution of the source currents. Anatomical information about the expected locations and orientations of the sources can be included in the source models. In particular, the sources can be assumed to be oriented perpendicular to the cortical surface. We introduce a minimum ℓ1‐norm estimation source modeling approach with loose orientation constraints (ℓ1LOC), which integrates the estimation of the orientation, location, and strength of the source currents into a cost function to jointly model the residual error and the ℓ1‐norm of the source estimates. Evaluation with simulated MEG data indicated that the ℓ1LOC method can provide low spatial dispersion, high localization accuracy, and high source detection rates. Application to somatosensory and auditory MEG data resulted in physiologically reasonable source distributions. The proposed ℓ1LOC method appears useful for incorporating anatomical information about the source orientations into sparse source estimation of MEG data. Hum Brain Mapp 34:2190–2201, 2013.

Multi-projection magnetic resonance inverse imaging of the human visuomotor system

Using highly parallel radiofrequency (RF) detection, magnetic resonance inverse imaging (InI) can achieve 100 ms temporal resolution with whole brain coverage. This is achieved by trading off partition encoding steps and thus spatial resolution for a higher acquisition rate. The reduced spatial information is estimated by solving under-determined inverse problems using RF coil sensitivity information. Here we propose multi projection inverse imaging (mInI) to combine different projection images to improve the spatial resolution of InI. Specifically, coronal, sagittal, and transverse projection images were acquired from different runs of the fMRI acquisitions using a 32-channel head coil array. Simulations show that mInI improves the quality of the instantaneous image reconstruction significantly. Going from one projection to three projections, the spatial resolution quantified by the full width at half maximum of the point-spread function (PSF) is improved from 2.6 pixels to 1.4 pixels (4 mm nominal resolution per pixel). Considering the shape of the PSF, the effective spatial resolution is improved from 16.9 pixels to 4.7 pixels. In vivo fMRI experiments using a two-choice reaction time tasks show visual and sensorimotor cortical activities spatially consistent with typical EPI data, yet mInI offers 100 ms temporal resolution with the whole brain coverage. The mInI data with three projections revealed that the sensorimotor cortex was activated 700 ms after the visual cortex. mInI can be applied to BOLD-contrast fMRI experiments to characterize the dynamics of the activated brain areas with a high spatiotemporal resolution.

Improving the spatial resolution of magnetic resonance inverse imaging via the blipped-CAIPI acquisition scheme

Using simultaneous acquisition from multiple channels of a radio-frequency (RF) coil array, magnetic resonance inverse imaging (InI) achieves functional MRI acquisitions at a rate of 100ms per whole-brain volume. InI accelerates the scan by leaving out partition encoding steps and reconstructs images by solving under-determined inverse problems using RF coil sensitivity information. Hence, the correlated spatial information available in the coil array causes spatial blurring in the InI reconstruction. Here, we propose a method that employs gradient blips in the partition encoding direction during the acquisition to provide extra spatial encoding in order to better differentiate signals from different partitions. According to our simulations, this blipped-InI (bInI) method can increase the average spatial resolution by 15.1% (1.3mm) across the whole brain and from 32.6% (4.2mm) in subcortical regions, as compared to the InI method. In a visual fMRI experiment, we demonstrate that, compared to InI, the spatial distribution of bInI BOLD response is more consistent with that of a conventional echo-planar imaging (EPI) at the level of individual subjects. With the improved spatial resolution, especially in subcortical regions, bInI can be a useful fMRI tool for obtaining high spatiotemporal information for clinical and cognitive neuroscience studies.

Suppression of irrelevant sounds during auditory working memory

Abstract Auditory working memory (WM) processing in everyday acoustic environments depends on our ability to maintain relevant information online in our minds, and to suppress interference caused by competing incoming stimuli. A challenge in communication settings is that the relevant content and irrelevant inputs may emanate from a common source, such as a talkative conversationalist. An open question is how the WM system deals with such interference. Will the distracters become inadvertently filtered before processing for meaning because the primary WM operations deplete all available processing resources? Or are they suppressed post perceptually, through an active control process? We tested these alternative hypotheses by measuring magnetoencephalography (MEG), EEG, and functional MRI (fMRI) during a phonetic auditory continuous performance task. Contextual WM maintenance load was manipulated by adjusting the number of “filler” letter sounds in‐between cue and target letter sounds. Trial‐to‐trial variability of pre‐ and post‐stimulus activations in fMRI‐informed cortical MEG/EEG estimates was analyzed within and across 14 subjects using generalized linear mixed effect (GLME) models. High contextual WM maintenance load suppressed left auditory cortex (AC) activations around 250–300 ms after the onset of irrelevant phonetic sounds. This effect coincided with increased 10–14 Hz alpha‐range oscillatory functional connectivity between the left dorsolateral prefrontal cortex (DLPFC) and left AC. Suppression of AC responses to irrelevant sounds during active maintenance of the task context also correlated with increased pre‐stimulus 7–15 Hz alpha power. Our results suggest that under high auditory WM load, irrelevant sounds are suppressed through a “late” active suppression mechanism, which prevents short‐term consolidation of irrelevant information without affecting the initial screening of potentially meaningful stimuli. The results also suggest that AC alpha oscillations play an inhibitory role during auditory WM processing. HighlightsWe studied distracter suppression under low/high auditory working memory (WM) load.High WM load reduced auditory cortex (AC) activations 250–300 ms after distracters.This involved increased prefrontal–AC alpha‐band connectivity and AC alpha activity.Under WM load, irrelevant sounds are suppressed through a “late”, active process.This allows initial screening but prevents consolidation of irrelevant information.