Optimization of wavelet coherence analysis as a measure of neural synchrony during hyperscanning using functional near-infrared spectroscopy.

SIGNIFICANCE: The expanding field of human social interaction is enabled by functional near-infrared spectroscopy (fNIRS) that acquires hemodynamic signals during live two-person interactions. These advances call for development of methods to quantify interactive processes. Aim: Wavelet coherence analysis has been applied to cross-brain neural coupling. However, fNIRS-specific computations have not been explored. This investigation determines the effects of global mean removal, wavelet equation, and choice of oxyhemoglobin versus deoxyhemoglobin signals. APPROACH: We compare signals with a known coherence with acquired signals to determine optimal computational approaches. The known coherence was calculated using three visual stimulation sequences of a contrast-reversing checkerboard convolved with the canonical hemodynamic response function. This standard was compared with acquired human fNIRS responses within visual cortex using the same sequences. RESULTS: Observed coherence was consistent with known coherence with highest correlations within the wavelength range between 10 and 20 s. Removal of the global mean improved the correlation irrespective of the specific equation for wavelet coherence, and the oxyhemoglobin signal was associated with a marginal correlation advantage. CONCLUSIONS: These findings provide both methodological and computational guidance that enhances the validity and interpretability of wavelet coherence analysis for fNIRS signals acquired during live social interactions

Co-localization of theta-band activity and hemodynamic responses during face perception: simultaneous electroencephalography and functional near-infrared spectroscopy recordings

Face-specific neural processes in the human brain have been localized to multiple anatomical structures and associated with diverse and dynamic social functions. The question of how various face-related systems and functions may be bound together remains an active area of investigation. We hypothesize that face processing may be associated with specific frequency band oscillations that serve to integrate distributed face processing systems. Using a multimodal imaging approach, including electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS), simultaneous signals were acquired during face and object picture viewing. As expected for face processing, hemodynamic activity in the right occipital face area (OFA) increased during face viewing compared to object viewing, and in a subset of participants, the expected N170 EEG response was observed for faces. Based on recently reported associations between the theta band and visual processing, we hypothesized that increased hemodynamic activity in a face processing area would also be associated with greater theta-band activity originating in the same area. Consistent with our hypothesis, theta-band oscillations were also localized to the right OFA for faces, whereas alpha- and beta-band oscillations were not. Together, these findings suggest that theta-band oscillations originating in the OFA may be part of the distributed face-specific processing mechanism

Activation in Right Dorsolateral Prefrontal Cortex Underlies Stuttering Anticipation

People who stutter learn to anticipate many of their overt stuttering events. Despite the critical role of anticipation, particularly how responses to anticipation shape stuttering behaviors, the neural bases associated with anticipation are unknown. We used a novel approach to identify anticipated and unanticipated words in 22 adult stutterers, which were produced in a delayed-response task while hemodynamic activity was measured using functional near infrared spectroscopy (fNIRS). Twenty-two control participants were included such that each individualized set of anticipated/unanticipated words was produced by one stutterer and one control. We conducted an analysis on the right dorsolateral prefrontal cortex (R-DLPFC) based on converging lines of evidence from the stuttering and cognitive control literatures. We also assessed connectivity between the R-DLPFC and right supramarginal gyrus (R-SMG), two key nodes of the frontoparietal network (FPN), to assess the role of cognitive control, particularly error-likelihood monitoring, in stuttering anticipation. All analyses focused on the five-second anticipation phase preceding the go signal to produce speech. Results indicate that anticipated words are associated with elevated activation in the R-DLPFC, and that compared to non-stutterers, stutterers exhibit greater activity in the R-DLPFC, irrespective of anticipation. Further, anticipated words are associated with reduced connectivity between the R-DLPFC and R-SMG. These findings highlight the potential roles of the R-DLPFC and the greater FPN as a neural substrate of stuttering anticipation. The results also support previous accounts of error-likelihood monitoring and action-stopping in stuttering anticipation. Overall, this work offers numerous directions for future research with clinical implications for targeted neuromodulation

Signal processing of functional NIRS data acquired during overt speaking

Functional near-infrared spectroscopy (fNIRS) offers an advantage over traditional functional imaging methods [such as functional magnetic resonance imaging (fMRI)] by allowing participants to move and speak relatively freely. However, neuroimaging while actively speaking has proven to be particularly challenging due to the systemic artifacts that tend to be located in the critical brain areas. To overcome these limitations and enhance the utility of fNIRS, we describe methods for investigating cortical activity during spoken language tasks through refinement of deoxyhemoglobin (deoxyHb) signals with principal component analysis (PCA) spatial filtering to remove global components. We studied overt picture naming and compared oxyhemoglobin (oxyHb) and deoxyHb signals with and without global component removal using general linear model approaches. Activity in Broca’s region and supplementary motor cortex was observed only when the filter was applied to the deoxyHb signal and was shown to be spatially comparable to fMRI data acquired using a similar task and to meta-analysis data. oxyHb signals did not yield expected activity in Broca’s region with or without global component removal. This study demonstrates the utility of a PCA spatial filter on the deoxyHb signal in revealing neural activity related to a spoken language task and extends applications of fNIRS to natural and ecologically valid conditions

Real-Time Eye-to-Eye Contact Is Associated With Cross-Brain Neural Coupling in Angular Gyrus

Direct eye contact between two individuals is a salient social behavior known to initiate and promote interpersonal interaction. However, the neural processes that underlie these live interactive behaviors and eye-to-eye contact are not well understood. The Dynamic Neural Coupling Hypothesis presents a general theoretical framework proposing that shared interactive behaviors are represented by cross-brain signal coherence. Using functional near-infrared spectroscopy (fNIRS) adapted for hyper scanning, we tested this hypothesis specifically for neural mechanisms associated with eye-to-eye gaze between human participants compared to similar direct eye-gaze at a dynamic video of a face and predicted that the coherence of neural signals between the two participants during reciprocal eye-to-eye contact would be greater than coherence observed during direct eye-gaze at a dynamic video for those signals originating in social and face processing systems. Consistent with this prediction cross-brain coherence was increased for signals within the angular gyrus (AG) during eye-to-eye contact relative to direct eye-gaze at a dynamic face video (p < 0.01). Further, activity in the right temporal-parietal junction (TPJ) was increased in the real eye-to-eye condition (p < 0.05, FDR corrected). Together, these findings advance a functional and mechanistic understanding of the AG and cross-brain neural coupling associated with real-time eye-to-eye contact

Comparison of short-channel separation and spatial domain filtering for removal of non-neural components in functional near-infrared spectroscopy signals

Significance: With the increasing popularity of functional near-infrared spectroscopy (fNIRS), the need to determine localization of the source and nature of the signals has grown. Aim: We compare strategies for removal of non-neural signals for a finger-thumb tapping task, which shows responses in contralateral motor cortex and a visual checkerboard viewing task that produces activity within the occipital lobe. Approach: We compare temporal regression strategies using short-channel separation to a spatial principal component (PC) filter that removes global signals present in all channels. For short-channel temporal regression, we compare non-neural signal removal using first and combined first and second PCs from a broad distribution of short channels to limited distribution on the forehead. Results: Temporal regression of non-neural information from broadly distributed short channels did not differ from forehead-only distribution. Spatial PC filtering provides results similar to short-channel separation using the temporal domain. Utilizing both first and second PCs from short channels removes additional non-neural information. Conclusions: We conclude that short-channel information in the temporal domain and spatial domain regression filtering methods remove similar non-neural components represented in scalp hemodynamics from fNIRS signals and that either technique is sufficient to remove non-neural components

Neural correlates of conflict between gestures and words: A domain-specific role for a temporal-parietal complex

The interpretation of social cues is a fundamental function of human social behavior, and resolution of inconsistencies between spoken and gestural cues plays an important role in successful interactions. To gain insight into these underlying neural processes, we compared neural responses in a traditional color/word conflict task and to a gesture/word conflict task to test hypotheses of domain-general and domain-specific conflict resolution. In the gesture task, recorded spoken words (“yes” and “no”) were presented simultaneously with video recordings of actors performing one of the following affirmative or negative gestures: thumbs up, thumbs down, head nodding (up and down), or head shaking (side-to-side), thereby generating congruent and incongruent communication stimuli between gesture and words. Participants identified the communicative intent of the gestures as either positive or negative. In the color task, participants were presented the words “red” and “green” in either red or green font and were asked to identify the color of the letters. We observed a classic “Stroop” behavioral interference effect, with participants showing increased response time for incongruent trials relative to congruent ones for both the gesture and color tasks. Hemodynamic signals acquired using functional near-infrared spectroscopy (fNIRS) were increased in the right dorsolateral prefrontal cortex (DLPFC) for incongruent trials relative to congruent trials for both tasks consistent with a common, domain-general mechanism for detecting conflict. However, activity in the left DLPFC and frontal eye fields and the right temporal-parietal junction (TPJ), superior temporal gyrus (STG), supramarginal gyrus (SMG), and primary and auditory association cortices was greater for the gesture task than the color task. Thus, in addition to domain-general conflict processing mechanisms, as suggested by common engagement of right DLPFC, socially specialized neural modules localized to the left DLPFC and right TPJ including adjacent homologous receptive language areas were engaged when processing conflicting communications. These findings contribute to an emerging view of specialization within the TPJ and adjacent areas for interpretation of social cues and indicate a role for the region in processing social conflict

Comparison of Oxyhemoglobin and Deoxyhemoglobin Signal Reliability With and Without Global Mean Removal for Digit Manipulation Motor Tasks

Functional near-infrared spectroscopy (fNIRS) could be well suited for clinical use, such as measuring neural activity before and after treatment; however, reliability and specificity of fNIRS signals must be ensured so that differences can be attributed to the intervention. This study compared the test–retest and longitudinal reliability of oxyhemoglobin and deoxyhemoglobin signals before and after spatial filtering. In the test–retest experiment, 14 participants were scanned on 2 days while performing four right-handed digit-manipulation tasks. Group results revealed greater test–retest reliability for oxyhemoglobin than deoxyhemoglobin signals and greater spatial specificity for the deoxyhemoglobin signals. To further characterize reliability, a longitudinal experiment was conducted in which two participants repeated the same motor tasks for 10 days. Beta values from the two tasks with the lowest and highest test–retest reliability, respectively, in the spatially filtered deoxyhemoglobin signal are reported as representative findings. Both test–retest and longitudinal methods confirmed that task and signal type influence reliability. Oxyhemoglobin signals were more reliable overall than deoxyhemoglobin, and removal of the global mean reduced reliability of both signals. Findings are consistent with the suggestion that systemic components most prevalent in the oxyhemoglobin signal may inflate reliability relative to the deoxyhemoglobin signal, which is less influenced by systemic factors

A cross-brain neural mechanism for human-to-human verbal communication

Neural mechanisms that mediate dynamic social interactions remain understudied despite their evolutionary significance. The interactive brain hypothesis proposes that interactive social cues are processed by dedicated brain substrates and provides a general theoretical framework for investigating the underlying neural mechanisms of social interaction. We test the specific case of this hypothesis proposing that canonical language areas are upregulated and dynamically coupled across brains during social interactions based on talking and listening. Functional near-infrared spectroscopy (fNIRS) was employed to acquire simultaneous deoxyhemoglobin (deOxyHb) signals of the brain on partners who alternated between speaking and listening while doing an Object Naming & Description task with and without interaction in a natural setting. Comparison of interactive and non-interactive conditions confirmed an increase in neural activity associated with Wernicke’s area including the superior temporal gyrus (STG) during interaction (P = 0.04). However, the hypothesis was not supported for Broca’s area. Cross-brain coherence determined by wavelet analyses of signals originating from the STG and the subcentral area was greater during interaction than non-interaction (P < 0.01). In support of the interactive brain hypothesis these findings suggest a dynamically coupled cross-brain neural mechanism dedicated to pathways that share interpersonal information

A fNIRS investigation of speech planning and execution in adults who stutter

Our study aimed to determine the neural correlates of speech planning and execution in adults who stutter (AWS). Fifteen AWS and 15 controls (CON) completed two tasks that either manipulated speech planning or execution processing loads. Functional near-infrared spectroscopy (fNIRS) was used to measure changes in blood flow concentrations during each task, thus providing an indirect measure of neural activity. An image-based reconstruction technique was used to analyze the results and facilitate their interpretation in the context of previous functional neuroimaging studies of AWS that used positron emission tomography (PET) or functional magnetic resonance imaging (fMRI). For planning, we compared neural activity associated with high versus low planning load in AWS and CON. For execution, we compared the neural activity associated with overt versus covert naming in AWS and CON. Broadly, group level effects corroborate previous PET/fMRI findings including under-activation in lefthemisphere perisylvian speech-language networks and over-activation in righthemisphere homologues. Increased planning load revealed atypical left-hemisphere activation in AWS, whereas increased execution load yielded atypical right frontotemporo-parietal and bilateral motor activation in AWS. Our results add to the limited literature differentiating speech planning versus execution processes in AWS