Intracranial stimulation and EEG feature analysis reveal affective salience network specialization.

Emotion is represented in limbic and prefrontal brain areas, herein termed the affective salience network (ASN). Within the ASN, there are substantial unknowns about how valence and emotional intensity are processed-specifically, which nodes are associated with affective bias (a phenomenon in which participants interpret emotions in a manner consistent with their own mood). A recently developed feature detection approach ('specparam') was used to select dominant spectral features from human intracranial electrophysiological data, revealing affective specialization within specific nodes of the ASN. Spectral analysis of dominant features at the channel level suggests that dorsal anterior cingulate (dACC), anterior insula and ventral-medial prefrontal cortex (vmPFC) are sensitive to valence and intensity, while the amygdala is primarily sensitive to intensity. Akaike information criterion model comparisons corroborated the spectral analysis findings, suggesting all four nodes are more sensitive to intensity compared to valence. The data also revealed that activity in dACC and vmPFC were predictive of the extent of affective bias in the ratings of facial expressions-a proxy measure of instantaneous mood. To examine causality of the dACC in affective experience, 130 Hz continuous stimulation was applied to dACC while patients viewed and rated emotional faces. Faces were rated significantly happier during stimulation, even after accounting for differences in baseline ratings. Together the data suggest a causal role for dACC during the processing of external affective stimuli.

Responses to Visual Speech in Human Posterior Superior Temporal Gyrus Examined with iEEG Deconvolution.

Experimentalists studying multisensory integration compare neural responses to multisensory stimuli with responses to the component modalities presented in isolation. This procedure is problematic for multisensory speech perception since audiovisual speech and auditory-only speech are easily intelligible but visual-only speech is not. To overcome this confound, we developed intracranial encephalography (iEEG) deconvolution. Individual stimuli always contained both auditory and visual speech, but jittering the onset asynchrony between modalities allowed for the time course of the unisensory responses and the interaction between them to be independently estimated. We applied this procedure to electrodes implanted in human epilepsy patients (both male and female) over the posterior superior temporal gyrus (pSTG), a brain area known to be important for speech perception. iEEG deconvolution revealed sustained positive responses to visual-only speech and larger, phasic responses to auditory-only speech. Confirming results from scalp EEG, responses to audiovisual speech were weaker than responses to auditory-only speech, demonstrating a subadditive multisensory neural computation. Leveraging the spatial resolution of iEEG, we extended these results to show that subadditivity is most pronounced in more posterior aspects of the pSTG. Across electrodes, subadditivity correlated with visual responsiveness, supporting a model in which visual speech enhances the efficiency of auditory speech processing in pSTG. The ability to separate neural processes may make iEEG deconvolution useful for studying a variety of complex cognitive and perceptual tasks.SIGNIFICANCE STATEMENT Understanding speech is one of the most important human abilities. Speech perception uses information from both the auditory and visual modalities. It has been difficult to study neural responses to visual speech because visual-only speech is difficult or impossible to comprehend, unlike auditory-only and audiovisual speech. We used intracranial encephalography deconvolution to overcome this obstacle. We found that visual speech evokes a positive response in the human posterior superior temporal gyrus, enhancing the efficiency of auditory speech processing.

Spatiotemporal dynamics of attentional orienting and reorienting revealed by fast optical imaging in occipital and parietal cortices.

The mechanisms of visuospatial attention are mediated by two distinct fronto-parietal networks: a bilateral dorsal network (DAN), involved in the voluntary orientation of visuospatial attention, and a ventral network (VAN), lateralized to the right hemisphere, involved in the reorienting of attention to unexpected, but relevant, stimuli. The present study consisted of two aims: 1) to characterize the spatio-temporal dynamics of attention and 2) to examine the predictive interactions between and within the two attention systems along with visual areas, by using fast optical imaging combined with Granger causality. Data were collected from young healthy participants performing a discrimination task in a Posner-like paradigm. Functional analyses revealed bilateral dorsal parietal (i.e. dorsal regions included in the DAN) and visual recruitment during orienting, highlighting a recursive predictive interplay between specific dorsal parietal regions and visual cortex. Moreover, we found that both attention networks are active during reorienting, together with visual cortex, highlighting a mutual interaction among dorsal and visual areas, which, in turn, predicts subsequent ventral activity. For attentional reorienting our findings indicate that dorsal and visual areas encode disengagement of attention from the attended location and trigger reorientation to the unexpected location. Ventral network activity could instead reflect post-perceptual maintenance of the internal model to generate and keep updated task-related expectations.

Regulating the Access to Awareness: Brain Activity Related to Probe-related and Spontaneous Reversals in Binocular Rivalry.

Research on the neural correlates of consciousness (NCC) has implicated an assortment of brain regions, ERP components, and network properties associated with visual awareness. Recently, the P3b ERP component has emerged as a leading NCC candidate. However, typical P3b paradigms depend on the detection of some stimulus change, making it difficult to separate brain processes elicited by the stimulus itself from those associated with updates or changes in visual awareness. Here we used binocular rivalry to ask whether the P3b is associated with changes in awareness even in the absence of changes in the object of awareness. We recorded ERPs during a probe-mediated binocular rivalry paradigm in which brief probes were presented over the image in either the suppressed or dominant eye to determine whether the elicited P3b activity is probe or reversal related. We found that the timing of P3b (but not its amplitude) was closely related to the timing of the report of a perceptual change rather than to the onset of the probe. This is consistent with the proposal that P3b indexes updates in conscious awareness, rather than being related to stimulus processing per se. Conversely, the probe-related P1 amplitude (but not its latency) was associated with reversal latency, suggesting that the degree to which the probe is processed increases the likelihood of a fast perceptual reversal. Finally, the response-locked P3b amplitude (but not its latency) was associated with the duration of an intermediate stage between reversals in which parts of both percepts coexist (piecemeal period). Together, the data suggest that the P3b reflects an update in consciousness and that the intensity of that process (as indexed by P3b amplitude) predicts how immediate that update is.

Psychometric Properties of a Novel Affective Bias Task and its Application in Clinical and Non-Clinical Populations.

To mitigate limitations in self-reported mood assessments, we introduce a novel affective bias task (ABT). The task quantifies instantaneous emotional state by leveraging the phenomenon of affective bias, in which people interpret external emotional stimuli in a manner consistent with their current emotional state. This study establishes task stability in measuring and tracking depressive symptoms in clinical and non-clinical populations. Initial assessment in a large non-clinical sample established normative ratings. Depressive symptoms were tracked relative to task performance in a non-clinical sample, as well as in a clinical cohort undergoing surgical evaluation for severe epilepsy. In both cohorts, a stronger negative affective bias was associated with higher Beck Depression Inventory (BDI-II) scores. The ABT exhibits high stability and interrater reliability, as well as construct validity in predicting depression levels in both cohorts, suggesting the task as a reliable proxy for mood and a diagnostic tool for detecting depressive symptoms.

Brain mechanisms underlying the emotion processing bias in treatment-resistant depression.

Depression is associated with a cognitive bias towards negative information and away from positive information. This biased emotion processing may underlie core depression symptoms, including persistent feelings of sadness or low mood and a reduced capacity to experience pleasure. The neural mechanisms responsible for this biased emotion processing remain unknown. Here, we had a unique opportunity to record stereotactic electroencephalography (sEEG) signals in the amygdala and prefrontal cortex (PFC) from 5 treatment-resistant depression (TRD) patients and 12 epilepsy patients (as control) while they participated in an affective bias task in which happy and sad faces were rated. First, compared with the control group, patients with TRD showed increased amygdala responses to sad faces in the early stage (around 300 ms) and decreased amygdala responses to happy faces in the late stage (around 600 ms) following the onset of faces. Further, during the late stage of happy face processing, alpha-band activity in PFC as well as alpha-phase locking between the amygdala and PFC were significantly greater in TRD patients compared to the controls. Second, after deep brain stimulation (DBS) delivered to bilateral subcallosal cingulate (SCC) and ventral capsule/ventral striatum (VC/VS), atypical amygdala and PFC processing of happy faces in TRD patients remitted toward the normative pattern. The increased amygdala activation during the early stage of sad face processing suggests an overactive bottom-up processing system in TRD. Meanwhile, the reduced amygdala response during the late stage of happy face processing could be attributed to inhibition by PFC through alpha-band oscillation, which can be released by DBS in SCC and VC/VS.

Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves.

The insula plays a fundamental role in a wide range of adaptive human behaviors, but its electrophysiological dynamics are poorly understood. Here, we used human intracranial electroencephalographic recordings to investigate the electrophysiological properties and hierarchical organization of spontaneous neuronal oscillations within the insula. We analyzed the neuronal oscillations of the insula directly and found that rhythms in the theta and beta frequency oscillations are widespread and spontaneously present. These oscillations are largely organized along the anterior-posterior (AP) axis of the insula. Both the left and right insula showed anterior--to-posterior decreasing gradients for the power of oscillations in the beta frequency band. The left insula also showed a posterior-to-anterior decreasing frequency gradient and an anterior-to-posterior decreasing power gradient in the theta frequency band. In addition to measuring the power of these oscillations, we also examined the phase of these signals across simultaneous recording channels and found that the insula oscillations in the theta and beta bands are traveling waves. The strength of the traveling waves in each frequency was positively correlated with the amplitude of each oscillation. However, the theta and beta traveling waves were uncoupled to each other in terms of phase and amplitude, which suggested that insular traveling waves in the theta and beta bands operate independently. Our findings provide new insights into the spatiotemporal dynamics and hierarchical organization of neuronal oscillations within the insula, which, given its rich connectivity with widespread cortical regions, indicates that oscillations and traveling waves have an important role in intrainsular and interinsular communications.

Imaging versus electrographic connectivity in human mood-related fronto-temporal networks.

BACKGROUND: The efficacy of psychiatric DBS is thought to be driven by the connectivity of stimulation targets with mood-relevant fronto-temporal networks, which is typically evaluated using diffusion-weighted tractography. OBJECTIVE: Leverage intracranial electrophysiology recordings to better predict the circuit-wide effects of neuromodulation to white matter targets. We hypothesize strong convergence between tractography-predicted structural connectivity and stimulation-induced electrophysiological responses. METHODS: Evoked potentials were elicited by single-pulse stimulation to two common DBS targets for treatment-resistant depression - the subcallosal cingulate (SCC) and ventral capsule/ventral striatum (VCVS) - in two patients undergoing DBS with stereo-electroencephalographic (sEEG) monitoring. Evoked potentials were compared with predicted structural connectivity between DBS leads and sEEG contacts using probabilistic, patient-specific diffusion-weighted tractography. RESULTS: Evoked potentials and tractography showed strong convergence in both patients in orbitofrontal, ventromedial prefrontal, and lateral prefrontal cortices for both SCC and VCVS stimulation targets. Low convergence was found in anterior cingulate (ACC), where tractography predicted structural connectivity from SCC targets but produced no evoked potentials during SCC stimulation. Further, tractography predicted no connectivity to ACC from VCVS targets, but VCVS stimulation produced robust evoked potentials. CONCLUSION: The two connectivity methods showed significant convergence, but important differences emerged with respect to the ability of tractography to predict electrophysiological connectivity between SCC and VCVS to regions of the mood-related network. This multimodal approach raises intriguing implications for the use of tractography in surgical targeting and provides new data to enhance our understanding of the network-wide effects of neuromodulation.

Probing the mechanisms of probe-mediated binocular rivalry.

Binocular rivalry occurs when incompatible images are presented simultaneously but separately to each eye. Perceptual dominance reverses over time such that one image temporarily dominates perception, while the other image is suppressed. Prior research has shown that briefly-presented probes modulate perception such that probes presented to the suppressed eye tend to produce shorter percept durations relative to when probes are presented to the dominant eye. This pattern suggests that probes strengthen the competitive strength of the image over which they appear. However, it remains unclear whether probe-modulated effects on binocular rivalry are equivalent across the visual field, in particular as a function of whether probes appear within the region of interocular conflict (i.e on-object) or outside the region of interocular conflict (i.e. off-object). We tested this by manipulating whether probes appeared on-object or off-object. We replicate prior work showing that suppressed-eye probes produce shorter percept durations relative to dominant-eye probes. Critically, however, we show that percept duration also varies as a function of whether probes appear on vs. off the rivalry objects; that is, differences in percept duration between suppressed-eye and dominant-eye probes were much larger for on-object than off-object probes. Importantly, however, the difference between suppressed-eye and dominant-eye probes was still significant for off-object probes. Together these results suggest dynamic mechanisms at work in probe-mediated rivalry, such that on-object probe effects are larger relative to smaller, yet reliable off-object effects.

The visual speech head start improves perception and reduces superior temporal cortex responses to auditory speech.

Visual information about speech content from the talker's mouth is often available before auditory information from the talker's voice. Here we examined perceptual and neural responses to words with and without this visual head start. For both types of words, perception was enhanced by viewing the talker's face, but the enhancement was significantly greater for words with a head start. Neural responses were measured from electrodes implanted over auditory association cortex in the posterior superior temporal gyrus (pSTG) of epileptic patients. The presence of visual speech suppressed responses to auditory speech, more so for words with a visual head start. We suggest that the head start inhibits representations of incompatible auditory phonemes, increasing perceptual accuracy and decreasing total neural responses. Together with previous work showing visual cortex modulation (Ozker et al., 2018b) these results from pSTG demonstrate that multisensory interactions are a powerful modulator of activity throughout the speech perception network.

Effects of attention to and awareness of preceding context tones on auditory streaming.

This study determined whether facilitation of auditory stream segregation could occur when facilitating context tones are accompanied by other sounds. Facilitation was measured as the likelihood of a repeated context tone that could match the low (A) or high (B) frequency of a repeating ABA test to increase the likelihood of hearing the test as segregated. We observed this type of facilitation when matching tones were alone, or with simultaneous bandpass noises or continuous speech, neither of which masked the tones. However, participants showed no streaming facilitation when a harmonic complex masked the context tones. Mistuning or desynchronizing the context tone relative to the rest of the complex did not facilitate streaming, despite the fact that the context tone was accessible to awareness and attention. Even presenting the context tone in a separate ear from the rest of the harmonic complex did not facilitate streaming, ruling out peripheral interference. Presenting the test as mistuned or desynchronized tones relative to complex tones eliminated the possibility that timbre changes from context to test interfered with facilitation resulting from the context. These results demonstrate the fragility of streaming facilitation and show that awareness of and attention to the context tones are not sufficient to overcome interference.