Oscillatory mechanisms supporting human cognition

By recording electrophysiological activity from electrodes on the surface of the brain or implanted in the depth of the brain, we are beginning to gain insights into the brain's oscillatory dynamics when humans perform cognitive tasks. The main goal was to acquire new knowledge about how different parts of the brain?s neural networks interact via oscillatory activity to enable working memory and attention. The method used is termed intracranial EEG and has not previously been used in cognitive research in Norway. Intracranial EEG is possible due to a unique population of patients that opt to have electrodes implanted in their brain. The electrodes allow localization of epileptic activity prior to surgical treatment for drug-resistant epilepsy. It is a powerful technique with unparalleled temporal (ms) and spatial (mm) resolution that permits detailed examination of the dynamic interplay of cortical processing within local- and across distant brain regions. We record from adult patients undergoing intracranial EEG at the Dept. of Neurosurgery, OUS. They participate in experiments designed to highlight the neural activity at work in directed attention and working memory. In conjunction with our intracranial patients, we also have the opportunity to record scalp EEG data from patients with focal brain lesions and from healthy volunteers. The integrated methodological approach is beneficial because it allows us to test whether lesions to specific frontal regions disrupt the cognitive functions in question, and whether those regions play a key role in modulating the task-related electrophysiological activity under study. By analyzing intracranial- and scalp EEG data of neurological patients and healthy controls we are able to examine how the brain manifests higher-order cognitive functions at varying levels of ability and what anatomical regions are required. The local team is composed of clinicians/researchers at the Dept. of Neurosurgery, OUS and the Dept. of Psychology, UiO. We collaborate closely with colleagues at UC Berkeley and data are collected at both OUS and US hospitals. Our international team has published articles on the neural basis of human?s ability to flexibly regulate attention and working memory. Selected examples are presented in the following: The role of the insular cortex for externally directed attention towards sounds is rarely studied due to its deep location in the brain. Using intracranial EEG we have examined whether the insula is activated when there is an unexpected change in a series of sound stimuli. We focused on activity in brain waves of high frequency, called the fast gamma band (75-145 Hz). Electrophysiological responses to auditory stimuli in general where seen in this frequency band in certain parts of the insula, whereas a small number of electrodes responded only when there was an unpredicted change in the sound sequence. The results showed that the insula forms a part of the auditory system and is engaged when stimuli deviate from an expected pattern (Blenkmann et al., 2019; Cortex). Another study examined the role of the lateral prefrontal cortex (LPFC) in both internally (own thoughts) and externally (the surroundings) directed attention. Healthy controls had increased power in the theta band during externally directed attention and increased alpha power during internally directed attention. Notably, patients with LPFC lesion showed no differences between the two states, providing evidence that damage to the LPFC leads to dysregulation of both attention types. This highlights the crucial role of the intact LPFC in supporting internally and externally directed attention (Kam et al., 2018; Neuroimage). Given the emerging role of theta band connectivity in attentional processes, we studied theta power correlation between DN and FPCN subsystems as a function of attention states using intracranial EEG. We found increased connectivity between DN and one of the FPCN systems during internally- compared to externally directed attention. This indicates that enhanced theta connectivity between the networks is a core electrophysiological mechanism underlying internally directed attention (Kam et al., 2019; Nature Human Behavior). We have also examined the neural basis of working memory. Dominant views focus on the prefrontal cortex (PFC), but other data suggest a role for the medial temporal lobe (MTL). To delineate whether these regions interact we recorded directly from PFC and MTL while patients performed a task that tested working memory for "what", "where", and "when" information. We found bidirectional communication between PFC and MTL during working memory. Our findings that rapid, dynamic interactions between these regions underlie working memory challenge dominant views on the central role of the PFC (Johnson et al., 2018; Plos Biology). More papers in progress are expected to provide new insights into the neurophysiological basis of core cognitive functions.

The project has led to establishment of human cognitive intracranial electrophysiology research in Norway. We have been able to address new questions regarding human cognition. Increased knowledge about oscillatory brain activity in relation to cognitive function is likely to be crucial for understanding oscillatory abnormalities associated with a variety of neurological and psychiatric disorders. The researchers have expanded their competence by working on new types of data. Collaboration between the Dept. of Psychology and the Dept. of Neurosurgery has resulted in mutual development of expertise and increased awareness about the importance of interaction between the sectors. Common infrastructure for handling of complex data has been developed, including data saving- and sharing facilities. The project has also led to establishment of interdisciplinary groups of researchers from several countries that plan future collaborations.

Over the last decade, a new and powerful frontier of neuroscience research has emerged, namely direct recordings from the surface of the human cerebral cortex with unparalleled temporal and spatial resolution. These direct cortical and intracortical recordings are referred to as electrocorticography (ECoG) and are obtained in patients implanted with intracranial electrodes typically for localization and treatment of medication refractory epilepsy. The current proposal is designed to establish the field of human electrocorticography in our country. With live recordings from conscious human brains, our overarching goal is to determine the oscillatory mechanisms underlying the fronto-parietal neural networks critical for attention and working memory, two cardinal aspects of human cognition. We propose a series of experiments to be conducted in Oslo, Stanford and UC Berkeley. Advanced signal analysis and connectivity measures will be utilized to determine the real-time neurophysiological mechanisms supporting attention and working memory. If funded, our proposal will lead to the establishment of human intracranial electrophysiology research in Norway, and will promote international cooperation with our colleagues at UC Berkeley and Stanford University towards deciphering the mechanisms of healthy brain function and how these might be disordered in patients with neurological and neuropsychiatric conditions.