Erik J. Aarnoutse

Neurophysiologic correlates of fMRI in human motor cortex.

The neurophysiological underpinnings of functional magnetic resonance imaging (fMRI) are not well understood. To understand the relationship between the fMRI blood oxygen level dependent (BOLD) signal and neurophysiology across large areas of cortex, we compared task related BOLD change during simple finger movement to brain surface electric potentials measured on a similar spatial scale using electrocorticography (ECoG). We found that spectral power increases in high frequencies (65–95 Hz), which have been related to local neuronal activity, colocalized with spatially focal BOLD peaks on primary sensorimotor areas. Independent of high frequencies, decreases in low frequency rhythms (<30 Hz), thought to reflect an aspect of cortical‐subcortical interaction, colocalized with weaker BOLD signal increase. A spatial regression analysis showed that there was a direct correlation between the amplitude of the task induced BOLD change on different areas of primary sensorimotor cortex and the amplitude of the high frequency change. Low frequency change explained an additional, different part of the spatial BOLD variance. Together, these spectral power changes explained a significant 36% of the spatial variance in the BOLD signal change (R2 = 0.36). These results suggest that BOLD signal change is largely induced by two separate neurophysiological mechanisms, one being spatially focal neuronal processing and the other spatially distributed low frequency rhythms. Hum Brain Mapp, 2011.

A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans

Functional mapping of eloquent cortex is often necessary prior to invasive brain surgery, but current techniques that derive this mapping have important limitations. In this article, we demonstrate the first comprehensive evaluation of a rapid, robust, and practical mapping system that uses passive recordings of electrocorticographic signals. This mapping procedure is based on the BCI2000 and SIGFRIED technologies that we have been developing over the past several years. In our study, we evaluated 10 patients with epilepsy from four different institutions and compared the results of our procedure with the results derived using electrical cortical stimulation (ECS) mapping. The results show that our procedure derives a functional motor cortical map in only a few minutes. They also show a substantial concurrence with the results derived using ECS mapping. Specifically, compared with ECS maps, a next-neighbor evaluation showed no false negatives, and only 0.46 and 1.10% false positives for hand and tongue maps, respectively. In summary, we demonstrate the first comprehensive evaluation of a practical and robust mapping procedure that could become a new tool for planning of invasive brain surgeries.

Brain–computer interfacing based on cognitive control

Brain–computer interfaces (BCIs) translate deliberate intentions and associated changes in brain activity into action, thereby offering patients with severe paralysis an alternative means of communication with and control over their environment. Such systems are not available yet, partly due to the high performance standard that is required. A major challenge in the development of implantable BCIs is to identify cortical regions and related functions that an individual can reliably and consciously manipulate. Research predominantly focuses on the sensorimotor cortex, which can be activated by imagining motor actions. However, because this region may not provide an optimal solution to all patients, other neuronal networks need to be examined. Therefore, we investigated whether the cognitive control network can be used for BCI purposes. We also determined the feasibility of using functional magnetic resonance imaging (fMRI) for noninvasive localization of the cognitive control network.

Fully Implanted Brain–Computer Interface in a Locked-In Patient with ALS

Options for people with severe paralysis who have lost the ability to communicate orally are limited. We describe a method for communication in a patient with late-stage amyotrophic lateral sclerosis (ALS), involving a fully implanted brain-computer interface that consists of subdural electrodes placed over the motor cortex and a transmitter placed subcutaneously in the left side of the thorax. By attempting to move the hand on the side opposite the implanted electrodes, the patient accurately and independently controlled a computer typing program 28 weeks after electrode placement, at the equivalent of two letters per minute. The brain-computer interface offered autonomous communication that supplemented and at times supplanted the patients eye-tracking device. (Funded by the Government of the Netherlands and the European Union; ClinicalTrials.gov number, NCT02224469 .).

Frequency specific spatial interactions in human electrocorticography: V1 alpha oscillations reflect surround suppression

Electrical brain signals are often decomposed into frequency ranges that are implicated in different functions. Using subdural electrocorticography (ECoG, intracranial EEG) and functional magnetic resonance imaging (fMRI), we measured frequency spectra and BOLD responses in primary visual cortex (V1) and intraparietal sulcus (IPS). In V1 and IPS, 30-120 Hz (gamma, broadband) oscillations allowed population receptive field (pRF) reconstruction comparable to fMRI estimates. Lower frequencies, however, responded very differently in V1 and IPS. In V1, broadband activity extends down to 3 Hz. In the 4-7 Hz (theta) and 18-30 Hz (beta) ranges broadband activity increases power during stimulation within the pRF. However, V1 9-12 Hz (alpha) frequency oscillations showed a different time course. The broadband power here is exceeded by a frequency-specific power increase during stimulation of the area outside the pRF. As such, V1 alpha oscillations reflected surround suppression of the pRF, much like negative fMRI responses. They were consequently highly localized, depending on stimulus and pRF position, and independent between nearby electrodes. In IPS, all 3-25 Hz oscillations were strongest during baseline recording and correlated between nearby electrodes, consistent with large-scale disengagement. These findings demonstrate V1 alpha oscillations result from locally active functional processes and relate these alpha oscillations to negative fMRI signals. They highlight that similar oscillations in different areas reflect processes with different functional roles. However, both of these roles of alpha seem to reflect suppression of spiking activity.

Propagating Neocortical Gamma Bursts Are Coordinated by Traveling Alpha Waves

Neocortical neuronal activity is characterized by complex spatiotemporal dynamics. Although slow oscillations have been shown to travel over space in terms of consistent phase advances, it is unknown how this phenomenon relates to neuronal activity in other frequency bands. We here present electrocorticographic data from three male and one female human subject and demonstrate that gamma power is phase locked to traveling alpha waves. Given that alpha activity has been proposed to coordinate neuronal processing reflected in the gamma band, we suggest that alpha waves are involved in coordinating neuronal processing in both space and time.

Functional MRI-based identification of brain areas involved in motor imagery for implantable brain–computer interfaces

For the development of minimally invasive brain-computer interfaces (BCIs), it is important to accurately localize the area of implantation. Using fMRI, we investigated which brain areas are involved in motor imagery. Twelve healthy subjects performed a motor execution and imagery task during separate fMRI and EEG measurements. fMRI results showed that during imagery, premotor and parietal areas were most robustly activated in individual subjects, but surprisingly, no activation was found in the primary motor cortex. EEG results showed that spectral power decreases in contralateral sensorimotor rhythms (8-24 Hz) during both movement and imagery. To further verify the involvement of the motor imagery areas found with fMRI, one epilepsy patient performed the same task during both fMRI and ECoG recordings. Significant ECoG low (8-24 Hz) and high (65-95 Hz) frequency power changes were observed selectively on premotor cortex and these co-localized with fMRI. During a subsequent BCI task, excellent performance (91%) was obtained based on ECoG power changes from the localized premotor area. These results indicate that other areas than the primary motor area may be more reliably activated during motor imagery. Specifically, the premotor cortex may be a better area to implant an invasive BCI.

Cortical theta wanes for language.

The role of low frequency oscillations in language areas is not yet understood. Using ECoG in six human subjects, we studied whether different language regions show prominent power changes in a specific rhythm, in similar manner as the alpha rhythm shows the most prominent power changes in visual areas. Brocas area and temporal language areas were localized in individual subjects using fMRI. In these areas, the theta rhythm showed the most pronounced power changes and theta power decreased significantly during verb generation. To better understand the role of this language-related theta decrease, we then studied the interaction between low frequencies and local neuronal activity reflected in high frequencies. Amplitude-amplitude correlations showed that theta power correlated negatively with high frequency activity, specifically across verb generation trials. Phase-amplitude coupling showed that during control trials, high frequency power was coupled to theta phase, but this coupling decreased significantly during verb generation trials. These results suggest a dynamic interaction between the neuronal mechanisms underlying the theta rhythm and local neuronal activity in language areas. As visual areas show a pronounced alpha rhythm that may reflect pulsed inhibition, language regions show a pronounced theta rhythm with highly similar features.

Mismatch Between Electrocortical Stimulation and Electrocorticography Frequency Mapping of Language

BACKGROUND Electrocortical Stimulation Mapping (ESM) is the gold standard for mapping eloquent cortex in neurosurgery. This technique, however, can cause seizures and requires good patient cooperation. Electrocorticography (ECoG) could replace ESM. Several studies have directly compared ESM and ECoG frequency mapping of language cortex, with mixed results. This may be due to ECoG mapping typically being limited to one or a few language tasks, potentially leading to underestimation of language representation. OBJECTIVE To evaluate the influence of the language task on the match between ECoG and ESM, we mapped language function based on episodes of spontaneous conversation with ECoG, and compared this with ESM data in eight epilepsy patients. A verb generation and picture naming task were used as reference standard. METHODS From the continuous ECoG and video registrations, periods of conversation were identified, distinguishing three conditions: speaking, listening and rest. A power-frequency analysis was done for each condition and the two language tasks. The match between ESM and ECoG frequency mapping was evaluated on the basis of sensitivity and specificity measures. RESULTS ECoG activation during spontaneous conversation and language tasks was seen in and around classic language areas. Comparing the electrodes activated in each condition with those indicated as language positive by ESM revealed that there was high specificity but relatively low sensitivity. CONCLUSION The relatively poor match between ESM and ECoG mapping is not improved by using spontaneous language.

Action preparation shapes processing in early visual cortex

Preparation for an action, such as grasping an object, is accompanied by an enhanced perception of the objects action-relevant features, such as orientation and size. Cortical feedback from motor planning areas to early visual areas may drive this enhanced perception. To examine whether action preparation modulates activity in early human visual cortex, subjects grasped or pointed to oriented objects while high-resolution fMRI data were acquired. Using multivoxel pattern analysis techniques, we could decode with >70% accuracy whether a grasping or pointing action was prepared from signals in visual cortex as early as V1. These signals in early visual cortex were observed even when actions were only prepared but not executed. Anterior parietal cortex, on the other hand, showed clearest modulation for actual movements. This demonstrates that preparation of actions, even without execution, modulates relevant neuronal populations in early visual areas.