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Intracranial electroencephalography (iEEG), also known as electrocorticography when using subdural grid electrodes or stereotactic EEG when using depth electrodes, is blossoming in various fields of human neuroscience. In this article, we highlight the potentials of iEEG in exploring functions of the human brain while also considering its limitations. The iEEG signal provides anatomically precise information about the selective engagement of neuronal populations at the millimeter scale and the temporal dynamics of their engagement at the millisecond scale. If several nodes of a given network are monitored simultaneously with implanted electrodes, the iEEG signals can also reveal information about functional interactions within and across networks during different stages of neural computation. As such, human iEEG can complement other methods of neuroscience beyond simply replicating what is already known, or can be known, from noninvasive lines of research in humans or from invasive recordings in nonhuman mammalian brains.

Neuroimaging evidence supports a role of the default mode network (DMN) in spontaneous thought and goal-driven internally oriented processes, such as recalling an autobiographical event, and has demonstrated its deactivation during focused, externally oriented attention. Recent work suggests that the DMN is not a homogeneous network but rather is composed of at least several subnetworks, which are engaged in distinct functions; however, it is still unclear if these different functions rely on the same neuronal populations. In this study, we used intracranial EEG to record from the posteromedial cortex (PMC), a core hub of the DMN, in 13 human subjects, during autobiographical memory retrieval (internally oriented), arithmetic processing (externally oriented), and cued rest (spontaneous thought), allowing us to measure activity from anatomically precise PMC sites with high temporal resolution. We observed a heterogeneous, yet spatially organized, pattern of activity across tasks. Many sites, primarily in the more ventral portion of PMC, were engaged during autobiographical recall and suppressed during arithmetic processing. Other more dorsal PMC sites were engaged during the cued-rest condition. Of these rest-active sites, some exhibited variable temporal dynamics across trials, possibly reflecting various forms of spontaneous thought, while others showed only transient activity at the beginning of cued-rest trials (i.e., after a switch from a task to cued rest), possibly involved in shifting the brain from a more focused to a more exploratory attentional state. These results suggest heterogeneity of function even within an individual node of the DMN.

In this review, we summarize the subjective experiential phenomena and behavioral changes that are caused by electrical stimulation of the cerebral cortex or subcortical nuclei in awake and conscious human subjects. Our comprehensive review contains a detailed summary of the data obtained from electrical brain stimulation (EBS) in humans in the last 100 years. Findings from the EBS studies may provide an additional layer of information about the neural correlates of cognition and behavior in healthy human subjects, or the neuroanatomy of illusions and hallucinations in patients with psychosis and the brain symptomatogenic zones in patients with epilepsy. We discuss some fundamental concepts, issues, and remaining questions that have defined the field of EBS, and review the current state of knowledge about the mechanism of action of EBS suggesting that the modulation of activity within a localized, but distributed, neuroanatomical network might explain the perceptual and behavioral phenomena that are reported during focal electrical stimulation of the human brain.

Neuroimaging evidence suggests that the default mode network (DMN) exhibits antagonistic activity with dorsal attention (DAN) and salience (SN) networks. Here we use human intracranial electroencephalography to investigate the behavioral relevance of fine-grained dynamics within and between these networks. The three networks show dissociable profiles of task-evoked electrophysiological activity, best captured in the high-frequency broadband (HFB; 70–170 Hz) range. On the order of hundreds of milliseconds, HFB responses peak fastest in the DAN, at intermediate speed in the SN, and slowest in the DMN. Lapses of attention (behavioral errors) are marked by distinguishable patterns of both pre- and post-stimulus HFB activity within each network. Moreover, the magnitude of temporally lagged, negative HFB coupling between the DAN and DMN (but not SN and DMN) is associated with greater sustained attention performance and is reduced during wakeful rest. These findings underscore the behavioral relevance of temporally delayed coordination between antagonistic brain networks. Brain imaging studies suggest that specific, large-scale, cortical networks show antagonistic activity with one another. Here, the authors studied the dynamics of these networks using implanted electrodes in the human brain, revealing that the coordination of inter-network dynamics on fast time scales relates to fluctuations in attention.

Language is classically thought to be supported by perisylvian cortical regions. Here we provide intracranial evidence linking the hippocampal complex to linguistic processing. We used direct recordings from the hippocampal structures to investigate whether theta oscillations, pivotal in memory function, track the amount of contextual linguistic information provided in sentences. Twelve participants heard sentences that were either constrained (“She locked the door with the”) or unconstrained (“She walked in here with the”) before presentation of the final word (“key”), shown as a picture that participants had to name. Hippocampal theta power increased for constrained relative to unconstrained contexts during sentence processing, preceding picture presentation. Our study implicates hippocampal theta oscillations in a language task using natural language associations that do not require memorization. These findings reveal that the hippocampal complex contributes to language in an active fashion, relating incoming words to stored semantic knowledge, a necessary process in the generation of sentence meaning.

Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. The authors show that neural oscillations establish dynamic communication networks within the frontal cortex and that these oscillations coordinate local neural activity with increasing cognitive control. Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. We utilized the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules resulted in greater frontal network theta phase encoding (4–8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80–150 Hz), which predicts trial-by-trial response times. Theta phase encoding coupled with high gamma amplitude during inter-regional information encoding, suggesting that inter-regional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

Neuroimaging studies of mentalizing (i.e., theory of mind) consistently implicate the default mode network (DMN). Nevertheless, the social cognitive functions of individual DMN regions remain unclear, perhaps due to limited spatiotemporal resolution in neuroimaging. Here we use electrocorticography (ECoG) to directly record neuronal population activity while 16 human participants judge the psychological traits of themselves and others. Self- and other-mentalizing recruit near-identical cortical sites in a common spatiotemporal sequence. Activations begin in the visual cortex, followed by temporoparietal DMN regions, then finally in medial prefrontal regions. Moreover, regions with later activations exhibit stronger functional specificity for mentalizing, stronger associations with behavioral responses, and stronger self/other differentiation. Specifically, other-mentalizing evokes slower and longer activations than self-mentalizing across successive DMN regions, implying lengthier processing at higher levels of representation. Our results suggest a common neurocognitive pathway for self- and other-mentalizing that follows a complex spatiotemporal gradient of functional specialization across DMN and beyond. The individual roles of default network regions in social thinking remain unclear. Using electrocorticography, the authors show a spatiotemporal hierarchy of neurocognitive specialization across temporoparietal and prefrontal default network regions.

Epilepsy is one of the most common neurological disorders affecting about 1% of the world population. For patients with focal seizures that cannot be treated with antiepileptic drugs, the common treatment is a surgical procedure for removal of the seizure onset zone (SOZ). In this work we introduce an algorithm for automatic localization of the seizure onset zone (SOZ) in epileptic patients based on electrocorticography (ECoG) recordings. The proposed algorithm builds upon the hypothesis that the abnormal excessive (or synchronous) neuronal activity in the brain leading to seizures starts in the SOZ and then spreads to other areas in the brain. Thus, when this abnormal activity starts, signals recorded at electrodes close to the SOZ should have a relatively large causal influence on the rest of the recorded signals. The SOZ localization is executed in two steps. First, the algorithm represents the set of electrodes using a directed graph in which nodes correspond to recording electrodes and the edges' weights quantify the pair-wise causal influence between the recorded signals. Then, the algorithm infers the SOZ from the estimated graph using a variant of the PageRank algorithm followed by a novel post-processing phase. Inference results for 19 patients show a close match between the SOZ inferred by the proposed approach and the SOZ estimated by expert neurologists (success rate of 17 out of 19).

The posteromedial cortex (PMC) is known to be a core node of the default mode network. Given its anatomical location and blood supply pattern, the effects of targeted disruption of this part of the brain are largely unknown. Here, we report a rare case of a patient (S19_137) with confirmed seizures originating within the PMC. Intracranial recordings confirmed the onset of seizures in the right dorsal posterior cingulate cortex, adjacent to the marginal sulcus, likely corresponding to Brodmann area 31. Upon the onset of seizures, the patient reported a reproducible sense of self-dissociation—a condition he described as a distorted awareness of the position of his body in space and feeling as if he had temporarily become an outside observer to his own thoughts, his “me” having become a separate entity that was listening to different parts of his brain speak to each other. Importantly, 50-Hz electrical stimulation of the seizure zone and a homotopical region within the contralateral PMC induced a subjectively similar state, reproducibly. We supplement our clinical findings with the definition of the patient’s network anatomy at sites of interest using cortico-cortical–evoked potentials, experimental and resting-state electrophysiological connectivity, and individual-level functional imaging. This rare case of patient S19_137 highlights the potential causal importance of the PMC for integrating self-referential information and provides clues for future mechanistic studies of self-dissociation in neuropsychiatric populations.