Neural dynamics of mindfulness meditation and hypnosis explored with intracranial EEG: A feasibility study.

PURPOSE: Intracranial electroencephalography (iEEG) offers a unique window on brain dynamics with excellent temporal and spatial resolution and is less prone to recording artefacts than surface EEG. This study used a within-subject design to explore the feasibility to compare iEEG data during mind wandering, mindfulness meditation and hypnosis. RESULTS: Three patients who had iEEG for clinical monitoring and who were new to mindfulness meditation and hypnosis were able to enter these states. We found non-specific and wide-spread amplitude modulations. Data-driven connectivity analysis revealed widespread connectivity patterns that were common across the three conditions. These were predominant in the low frequencies (delta, theta and alpha) and characterised by positively correlated activity. Connectivity patterns that were unique to the three conditions predominated in the gamma band, one third of the correlations in these patterns were negative. CONCLUSIONS: This study is the first to support the feasibility of a direct comparison of the neural correlates of mindfulness meditation and hypnosis using iEEG. These modulations may reflect the complex interplay between different known brain networks, and warrant further functional investigations in particular in the gamma band.

Identifying task-relevant spectral signatures of perceptual categorization in the human cortex.

Human brain has developed mechanisms to efficiently decode sensory information according to perceptual categories of high prevalence in the environment, such as faces, symbols, objects. Neural activity produced within localized brain networks has been associated with the process that integrates both sensory bottom-up and cognitive top-down information processing. Yet, how specifically the different types and components of neural responses reflect the local networks' selectivity for categorical information processing is still unknown. In this work we train Random Forest classification models to decode eight perceptual categories from broad spectrum of human intracranial signals (4-150 Hz, 100 subjects) obtained during a visual perception task. We then analyze which of the spectral features the algorithm deemed relevant to the perceptual decoding and gain the insights into which parts of the recorded activity are actually characteristic of the visual categorization process in the human brain. We show that network selectivity for a single or multiple categories in sensory and non-sensory cortices is related to specific patterns of power increases and decreases in both low (4-50 Hz) and high (50-150 Hz) frequency bands. By focusing on task-relevant neural activity and separating it into dissociated anatomical and spectrotemporal groups we uncover spectral signatures that characterize neural mechanisms of visual category perception in human brain that have not yet been reported in the literature.

Activations of deep convolutional neural networks are aligned with gamma band activity of human visual cortex.

Recent advances in the field of artificial intelligence have revealed principles about neural processing, in particular about vision. Previous work demonstrated a direct correspondence between the hierarchy of the human visual areas and layers of deep convolutional neural networks (DCNN) trained on visual object recognition. We use DCNN to investigate which frequency bands correlate with feature transformations of increasing complexity along the ventral visual pathway. By capitalizing on intracranial depth recordings from 100 patients we assess the alignment between the DCNN and signals at different frequency bands. We find that gamma activity (30-70 Hz) matches the increasing complexity of visual feature representations in DCNN. These findings show that the activity of the DCNN captures the essential characteristics of biological object recognition not only in space and time, but also in the frequency domain. These results demonstrate the potential that artificial intelligence algorithms have in advancing our understanding of the brain.

Effective Connectivity between Ventral Occipito-Temporal and Ventral Inferior Frontal Cortex during Lexico-Semantic Processing. A Dynamic Causal Modeling Study.

It has been suggested that dorsal and ventral pathways support distinct aspects of language processing. Yet, the full extent of their involvement and their inter-regional connectivity in visual word recognition is still unknown. Studies suggest that they might reflect the dual-route model of reading, with the dorsal pathway more involved in grapho-phonological conversion during phonological tasks, and the ventral pathway performing lexico-semantic access during semantic tasks. Furthermore, this subdivision is also suggested at the level of the inferior frontal cortex, involving ventral and dorsal parts for lexico-semantic and phonological processing, respectively. In the present study, we assessed inter-regional brain connectivity and task-induced modulations of brain activity during a phoneme detection and semantic categorization tasks, using fMRI in healthy subject. We used a dynamic causal modeling approach to assess inter-regional connectivity and task demand modulation within the dorsal and ventral pathways, including the following network components: the ventral occipito-temporal cortex (vOTC; dorsal and ventral), the superior temporal gyrus (STG; dorsal), the dorsal inferior frontal gyrus (dIFG; dorsal), and the ventral IFG (vIFG; ventral). We report three distinct inter-regional interactions supporting orthographic information transfer from vOTC to other language regions (vOTC -> STG, vOTC -> vIFG and vOTC -> dIFG) regardless of task demands. Moreover, we found that (a) during semantic processing (direct ventral pathway) the vOTC -> vIFG connection strength specifically increased and (b) a lack of modulation of the vOTC -> dIFG connection strength by the task that could suggest a more general involvement of the dorsal pathway during visual word recognition. Results are discussed in terms of anatomo-functional connectivity of visual word recognition network.

Selective Neural Synchrony Suppression as a Forward Gatekeeper to Piecemeal Conscious Perception.

The emergence of conscious visual perception is assumed to ignite late (∼250 ms) gamma-band oscillations shortly after an initial (∼100 ms) forward sweep of neural sensory (nonconscious) information. However, this neural evidence is not utterly congruent with rich behavioral data which rather point to piecemeal (i.e., graded) perceptual processing. To address the unexplored neural mechanisms of piecemeal ignition of conscious perception, hierarchical script sensitivity of the putative visual word form area (VWFA) was exploited to signal null (i.e., sensory), partial (i.e., letter-level), and full (i.e., word-level) conscious perception. Two magnetoencephalography experiments were conducted in which healthy human participants viewed masked words (Experiment I: active task, Dutch words; Experiment II: passive task, Hebrew words) while high-frequency (broadband gamma) brain activity was measured. Findings revealed that piecemeal conscious perception did not ignite a linear piecemeal increase in oscillations. Instead, whereas late (∼250 ms) gamma-band oscillations signaled full conscious perception (i.e., word-level), partial conscious perception (i.e., letter-level) was signaled via the inhibition of the early (∼100 ms) forward sweep. This inhibition regulates the downstream broadcast to filter out irrelevant (i.e., masks) information. The findings thus highlight a local (VWFA) gatekeeping mechanism for conscious perception, operating by filtering out and in selective percepts.

Neural repetition suppression in ventral occipito-temporal cortex occurs during conscious and unconscious processing of frequent stimuli.

Stimulus repetition can produce neural response attenuation in stimulus-category selective networks within the occipito-temporal lobe. It is hypothesized that this neural suppression reflects the functional sharpening of local neuronal assemblies which boosts information processing efficiency. This neural suppression phenomenon has been mainly reported during conditions of conscious stimulus perception. The question remains whether frequent stimuli processed in the absence of conscious perception also induce repetition suppression in those specialized networks. Using rare intracranial EEG recordings in the ventral occipito-temporal cortex (VOTC) of human epileptic patients we investigated neural repetition suppression in conditions of conscious and unconscious visual processing of words. To this end, we used an orthogonal design manipulating respectively stimulus repetition (frequent vs. unique stimuli) and conscious perception (masked vs. unmasked stimuli). By measuring the temporal dynamics of high-frequency broadband gamma activity in VOTC and testing for main and interaction effects, we report that early processing of words in word-form selective networks exhibits a temporal cascade of modulations by stimulus repetition and masking: neuronal attenuation initially is observed in response to repeated words (irrespective of consciousness), that is followed by a second modulation contingent upon word reportability (irrespective of stimulus repetition). Later on (>300ms post-stimulus), a significant effect of conscious perception on the extent of repetition suppression was observed. The temporal dynamics of consciousness, the recognition memory processes and their interaction revealed in this study advance our understanding of their contributions to the neural mechanisms of word processing in VOTC.

Functional selectivity in the human occipitotemporal cortex during natural vision: evidence from combined intracranial EEG and eye-tracking.

Eye movements are a constant and essential component of natural vision, yet, most of our knowledge about the human visual system comes from experiments that restrict them. This experimental constraint is mostly in place to control visual stimuli presentation and to avoid artifacts in non-invasive measures of brain activity, however, this limitation can be overcome with intracranial EEG (iEEG) recorded from epilepsy patients. Moreover, the high-frequency components of the iEEG signal (between about 50 and 150Hz) can provide a proxy of population-level spiking activity in any cortical area during free-viewing. We combined iEEG with high precision eye-tracking to study fine temporal dynamics and functional specificity in the fusiform face (FFA) and visual word form area (VWFA) while patients inspected natural pictures containing faces and text. We defined the first local measure of visual (electrophysiological) responsiveness adapted to free-viewing in humans: amplitude modulations in the high-frequency activity range (50-150Hz) following fixations (fixation-related high-frequency response). We showed that despite the large size of receptive fields in the ventral occipito-temporal cortex, neural activity during natural vision of realistic cluttered scenes is mostly dependent upon the category of the foveated stimulus - suggesting that category-specificity is preserved during free-viewing and that attention mechanisms might filter out the influence of objects surrounding the fovea.

Intracranial spectral amplitude dynamics of perceptual suppression in fronto-insular, occipito-temporal, and primary visual cortex.

If conscious perception requires global information integration across active distant brain networks, how does the loss of conscious perception affect neural processing in these distant networks? Pioneering studies on perceptual suppression (PS) described specific local neural network responses in primary visual cortex, thalamus and lateral prefrontal cortex of the macaque brain. Yet the neural effects of PS have rarely been studied with intracerebral recordings outside these cortices and simultaneously across distant brain areas. Here, we combined (1) a novel experimental paradigm in which we produced a similar perceptual disappearance and also re-appearance by using visual adaptation with transient contrast changes, with (2) electrophysiological observations from human intracranial electrodes sampling wide brain areas. We focused on broadband high-frequency (50-150 Hz, i.e., gamma) and low-frequency (8-24 Hz) neural activity amplitude modulations related to target visibility and invisibility. We report that low-frequency amplitude modulations reflected stimulus visibility in a larger ensemble of recording sites as compared to broadband gamma responses, across distinct brain regions including occipital, temporal and frontal cortices. Moreover, the dynamics of the broadband gamma response distinguished stimulus visibility from stimulus invisibility earlier in anterior insula and inferior frontal gyrus than in temporal regions, suggesting a possible role of fronto-insular cortices in top-down processing for conscious perception. Finally, we report that in primary visual cortex only low-frequency amplitude modulations correlated directly with perceptual status. Interestingly, in this sensory area broadband gamma was not modulated during PS but became positively modulated after 300 ms when stimuli were rendered visible again, suggesting that local networks could be ignited by top-down influences during conscious perception.

Temporal components in the parahippocampal place area revealed by human intracerebral recordings.

Many high-level visual regions exhibit complex patterns of stimulus selectivity that make their responses difficult to explain in terms of a single cognitive mechanism. For example, the parahippocampal place area (PPA) responds maximally to environmental scenes during fMRI studies but also responds strongly to nonscene landmark objects, such as buildings, which have a quite different geometric structure. We hypothesized that PPA responses to scenes and buildings might be driven by different underlying mechanisms with different temporal profiles. To test this, we examined broadband γ (50-150 Hz) responses from human intracerebral electroencephalography recordings, a measure that is closely related to population spiking activity. We found that the PPA distinguished scene from nonscene stimuli in ∼80 ms, suggesting the operation of a bottom-up process that encodes scene-specific visual or geometric features. In contrast, the differential PPA response to buildings versus nonbuildings occurred later (∼170 ms) and may reflect a delayed processing of spatial or semantic features definable for both scenes and objects, perhaps incorporating signals from other cortical regions. Although the response preferences of high-level visual regions are usually interpreted in terms of the operation of a single cognitive mechanism, these results suggest that a more complex picture emerges when the dynamics of recognition are considered.

Alpha-band suppression in the visual word form area as a functional bottleneck to consciousness.

The current state of empirical investigations refers to consciousness as an all-or-none phenomenon. However, a recent theoretical account opens up this perspective by proposing a partial level (between nil and full) of conscious perception. In the well-studied case of single-word reading, short-lived exposure can trigger incomplete word-form recognition wherein letters fall short of forming a whole word in one's conscious perception thereby hindering word-meaning access and report. Hence, the processing from incomplete to complete word-form recognition straightforwardly mirrors a transition from partial to full-blown consciousness. We therefore hypothesized that this putative functional bottleneck to consciousness (i.e. the perceptual boundary between partial and full conscious perception) would emerge at a major key hub region for word-form recognition during reading, namely the left occipito-temporal junction. We applied a real-time staircase procedure and titrated subjective reports at the threshold between partial (letters) and full (whole word) conscious perception. This experimental approach allowed us to collect trials with identical physical stimulation, yet reflecting distinct perceptual experience levels. Oscillatory brain activity was monitored with magnetoencephalography and revealed that the transition from partial-to-full word-form perception was accompanied by alpha-band (7-11 Hz) power suppression in the posterior left occipito-temporal cortex. This modulation of rhythmic activity extended anteriorly towards the visual word form area (VWFA), a region whose selectivity for word-forms in perception is highly debated. The current findings provide electrophysiological evidence for a functional bottleneck to consciousness thereby empirically instantiating a recently proposed partial perspective on consciousness. Moreover, the findings provide an entirely new outlook on the functioning of the VWFA as a late bottleneck to full-blown conscious word-form perception.

How silent is silent reading? Intracerebral evidence for top-down activation of temporal voice areas during reading.

As you might experience it while reading this sentence, silent reading often involves an imagery speech component: we can hear our own "inner voice" pronouncing words mentally. Recent functional magnetic resonance imaging studies have associated that component with increased metabolic activity in the auditory cortex, including voice-selective areas. It remains to be determined, however, whether this activation arises automatically from early bottom-up visual inputs or whether it depends on late top-down control processes modulated by task demands. To answer this question, we collaborated with four epileptic human patients recorded with intracranial electrodes in the auditory cortex for therapeutic purposes, and measured high-frequency (50-150 Hz) "gamma" activity as a proxy of population level spiking activity. Temporal voice-selective areas (TVAs) were identified with an auditory localizer task and monitored as participants viewed words flashed on screen. We compared neural responses depending on whether words were attended or ignored and found a significant increase of neural activity in response to words, strongly enhanced by attention. In one of the patients, we could record that response at 800 ms in TVAs, but also at 700 ms in the primary auditory cortex and at 300 ms in the ventral occipital temporal cortex. Furthermore, single-trial analysis revealed a considerable jitter between activation peaks in visual and auditory cortices. Altogether, our results demonstrate that the multimodal mental experience of reading is in fact a heterogeneous complex of asynchronous neural responses, and that auditory and visual modalities often process distinct temporal frames of our environment at the same time.

Long-distance amplitude correlations in the high γ band reveal segregation and integration within the reading network.

Reading sentences involves a distributed network of brain regions acting in concert surrounding the left sylvian fissure. The mechanisms of neural communication underlying the extraction and integration of verbal information across subcomponents of this reading network are still largely unknown. We recorded intracranial EEG activity in 12 epileptic human patients performing natural sentence reading and analyzed long-range corticocortical interactions between local neural activations. During a simple task contrasting semantic, phonological, and purely visual processes, we found process-specific neural activity elicited at the single-trial level, characterized by energy increases in a broad gamma band (40-150 Hz). Correlation analysis between task-induced gamma-band activations revealed a selective fragmentation of the network into specialized subnetworks supporting sentence-level semantic analysis and phonological processing. We extend the implications of our results beyond reading, to propose that gamma-band amplitude correlations might constitute a fundamental mechanism for large-scale neural integration during high-level cognition.

Efficient "pop-out" visual search elicits sustained broadband γ activity in the dorsal attention network.

An object that differs markedly from its surrounding-for example, a red cherry among green leaves-seems to pop out effortlessly in our visual experience. The rapid detection of salient targets, independently of the number of other items in the scene, is thought to be mediated by efficient search brain mechanisms. It is not clear, however, whether efficient search is actually an "effortless" bottom-up process or whether it also involves regions of the prefrontal cortex generally associated with top-down sustained attention. We addressed this question with intracranial EEG (iEEG) recordings designed to identify brain regions underlying a classic visual search task and correlate neural activity with target detection latencies on a trial-by-trial basis with high temporal precision recordings of these regions in epileptic patients. The spatio-temporal dynamics of single-trial spectral analysis of iEEG recordings revealed sustained energy increases in a broad gamma band (50-150 Hz) throughout the duration of the search process in the entire dorsal attention network both in efficient and inefficient search conditions. By contrast to extensive theoretical and experimental indications that efficient search relies exclusively on transient bottom-up processes in visual areas, we found that efficient search is mediated by sustained gamma activity in the dorsal lateral prefrontal cortex and the anterior cingulate cortex, alongside the superior parietal cortex and the frontal eye field. Our findings support the hypothesis that active visual search systematically involves the frontal-parietal attention network and therefore, executive attention resources, regardless of target saliency.

Reading the mind's eye: online detection of visuo-spatial working memory and visual imagery in the inferior temporal lobe.

Several brain regions involved in visual perception have been shown to also participate in non-sensory cognitive processes of visual representations. Here we studied the role of ventral visual pathway areas in visual imagery and working memory. We analyzed intracerebral EEG recordings from the left inferior temporal lobe of an epileptic patient during working memory tasks and mental imagery. We found that high frequency gamma-band activity (50-150 Hz) in the inferior temporal gyrus (ITG) increased with memory load only during visuo-spatial, but not verbal, working memory. Using a real-time set-up to measure and visualize gamma-band activity online--BrainTV--we found a systematic activity increase in ITG when the patient was visualizing a letter (visual imagery), but not during perception of letters. In contrast, only 7 mm more medially, neurons located in the fusiform gyrus exhibited a complete opposite pattern, responding during verbal working memory retention and letter presentation, but not during imagery or visuo-spatial working memory maintenance. Talairach coordinates indicate that the fusiform contact site corresponds to the word form area, suggesting that this region has a role not only in processing letter-strings, but also in working memory retention of verbal information. We conclude that neural networks supporting imagination of a visual element are not necessarily the same as those underlying perception of that element. Additionally, we present evidence that gamma-band activity in the inferior temporal lobe, can be used as a direct measure of the efficiency of top-down attentional control over visual areas with implications for the development of novel brain-computer interfaces. Finally, by just reading gamma-band activity in these two recording sites, it is possible to determine, accurately and in real-time, whether a given memory content is verbal or visuo-spatial.

Transient suppression of broadband gamma power in the default-mode network is correlated with task complexity and subject performance.

Task performance is associated with increased brain metabolism but also with prominent deactivation in specific brain structures known as the default-mode network (DMN). The role of DMN deactivation remains enigmatic in part because its electrophysiological correlates, temporal dynamics, and link to behavior are poorly understood. Using extensive depth electrode recordings in humans, we provide first electrophysiological evidence for a direct correlation between the dynamics of power decreases in the DMN and individual subject behavior. We found that all DMN areas displayed transient suppressions of broadband gamma (60-140 Hz) power during performance of a visual search task and, critically, we show for the first time that the millisecond range duration and extent of the transient gamma suppressions are correlated with task complexity and subject performance. In addition, trial-by-trial correlations revealed that spatially distributed gamma power increases and decreases formed distinct anticorrelated large-scale networks. Beyond unraveling the electrophysiological basis of DMN dynamics, our results suggest that, rather than indicating a mere switch to a global exteroceptive mode, DMN deactivation encodes the extent and efficiency of our engagement with the external world. Furthermore, our findings reveal a pivotal role for broadband gamma modulations in the interplay between task-positive and task-negative networks mediating efficient goal-directed behavior and facilitate our understanding of the relationship between electrophysiology and neuroimaging studies of intrinsic brain networks.

Direct evidence for two different neural mechanisms for reading familiar and unfamiliar words: an intra-cerebral EEG study.

After intensive practice, unfamiliar letter strings become familiar words and reading speed increases strikingly from a slow processing to a fast and with more global recognition of words. While this effect has been well documented at the behavioral level, its neural underpinnings are still unclear. The question is how the brain modulates the activity of the reading network according to the novelty of the items. Several models have proposed that familiar and unfamiliar words are not processed by separate networks but rather by common regions operating differently according to familiarity. This hypothesis has proved difficult to test at the neural level because the effects of familiarity and length on reading occur (a) on a millisecond scale, shorter than the resolution of fMRI and (b) in regions which cannot be isolated with non-invasive EEG or MEG. We overcame these limitations by using invasive intra-cerebral EEG recording in epileptic patients. Neural activity (gamma-band responses, between 50 and 150 Hz) was measured in three major nodes of reading network - left inferior frontal, supramarginal, and inferior temporo-occipital cortices - while patients silently read familiar (words) and unfamiliar (pseudo-words) items of two lengths (short composed of one-syllable vs. long composed of three-syllables). While all items elicited strong neural responses in the three regions, we found that the duration of the neural response increases with length only for pseudo-words, in direct relation to orthographic-to-phonological conversion. Our results validate at the neural level the hypothesis that all words are processed by a common network operating more or less efficiently depending on words' novelty.

Intracerebral γ modulations reveal interaction between emotional processing and action outcome evaluation in the human orbitofrontal cortex.

The orbitofrontal cortex (OFC) plays a key role not only in processing emotions but also in monitoring performance outcome. Although the neuroanatomical substrates underlying each of the two processes have been extensively investigated, they have predominantly been probed separately and therefore a precise knowledge of the functional overlap within the multiple OFC sub-portions involved is still lacking. Here, we explore the neural dynamics mediating performance monitoring and emotional processing using direct intracranial EEG (iEEG) recordings from multiple OFC sites of an epileptic patient. Neural activity was recorded during two experiments. The first task required processing of emotional faces and the second investigated action outcome evaluation based on a visual feedback on the subject's performance. Task-related neural dynamics were assessed using modulations of high frequency responses in the gamma-band (50-150Hz). Our results reveal that processing negative facial emotions as well as receiving negative feedback both elicited gamma-band responses in the lateral OFC. By contrast, the mid-OFC was selectively activated for positive feedback. Furthermore, we also found significant gamma-band deactivation in the gyrus rectus during processing of negative feedback. Our findings provide novel evidence for an intricate valence-selective interaction between the networks mediating emotion processing and performance monitoring in human OFC and support the hypothesis of a tight relationship between gamma-band activity and behavior.

Exploring the electrophysiological correlates of the default-mode network with intracerebral EEG.

While functional imaging studies allow for a precise spatial characterization of resting state networks, their neural correlates and thereby their fine-scale temporal dynamics remain elusive. A full understanding of the mechanisms at play requires input from electrophysiological studies. Here, we discuss human and non-human primate electrophysiological data that explore the neural correlates of the default-mode network. Beyond the promising findings obtained with non-invasive approaches, emerging evidence suggests that invasive recordings in humans will be crucial in order to elucidate the neural correlates of the brain's default-mode function. In particular, we contend that stereotactic-electroencephalography, which consists of implanting multiple depth electrodes for pre-surgical evaluation in drug-resistant epilepsy, is particularly suited for this endeavor. We support this view by providing rare data from depth recordings in human posterior cingulate cortex and medial prefrontal cortex that show transient neural deactivation during task-engagement.