Nathan E. Crone

Induced electrocorticographic gamma activity during auditory perception

Abstract Objective : To define the spatial, temporal, and functional characteristics of induced gamma (>30 Hz) activity during functional activation of the left superior temporal gyrus. Methods : Electrocorticographic (ECoG) recordings were made in 4 clinical subjects during auditory tone and phoneme discrimination tasks, and event-related changes in the ECoG band power were calculated. The topography and temporal sequence of event-related power changes in different gamma bands were contrasted with those of auditory evoked potentials (AEPs), and with those of event-related power changes in the alpha band (8–12 Hz). Results : Auditory stimuli induced a broadband power augmentation that included 40 Hz, as well as higher (80–100 Hz) gamma frequencies. The topography of gamma augmentation was similar, but not identical, to that of the AEP, and was more focused than that of alpha power suppression. Its temporal onset coincided with the N100, but outlasted it. Phonemes produced greater gamma augmentation than tones, while a similar difference was not observed in the N100. Conclusions : Auditory perception induces ECoG gamma activity not only at 40 Hz, but also in higher gamma frequencies. This activity appears to be an index of cortical activation that reflects task-specific processing in the human auditory cortex more closely than the AEP or alpha power suppression.

Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in Electrocorticography

Recent studies using electrocorticographic (ECoG) recordings in humans have shown that functional activation of cortex is associated with an increase in power in the high-gamma frequency range (∼60–200 Hz). Here we investigate the neural correlates of this high-gamma activity in local field potential (LFP). Single units and LFP were recorded with microelectrodes from the hand region of macaque secondary somatosensory cortex while vibrotactile stimuli of varying intensities were presented to the hand. We found that high-gamma power in the LFP was strongly correlated with the average firing rate recorded by the microelectrodes, both temporally and on a trial-by-trial basis. In comparison, the correlation between firing rate and low-gamma power (40–80 Hz) was much smaller. To explore the potential effects of neuronal firing on ECoG, we developed a model to estimate ECoG power generated by different firing patterns of the underlying cortical population and studied how ECoG power varies with changes in firing rate versus the degree of synchronous firing between neurons in the population. Both an increase in firing rate and neuronal synchrony increased high-gamma power in the simulated ECoG data. However, ECoG high-gamma activity was much more sensitive to increases in neuronal synchrony than firing rate.

Reconstructing speech from human auditory cortex.

Direct brain recordings from neurosurgical patients listening to speech reveal that the acoustic speech signals can be reconstructed from neural activity in auditory cortex.

Electrocorticographic gamma activity during word production in spoken and sign language

Objective: To investigate the functional-neuroanatomic substrates of word production using signed versus spoken language. Methods: The authors studied single-word processing with varying input and output modalities in a 38-year-old woman with normal hearing and speech who had become proficient in sign language 8 years before developing intractable epilepsy. Subdural electrocorticography (ECoG) was performed during picture naming and word reading (visual inputs) and word repetition (auditory inputs); these tasks were repeated with speech and with sign language responses. Cortical activation was indexed by event-related power augmentation in the 80- to 100-Hz gamma band, and was compared with general principles of functional anatomy and with subject-specific maps of the same or similar tasks using electrical cortical stimulation (ECS). Results: Speech outputs activated tongue regions of the sensorimotor cortex, and sign outputs activated hand regions. In addition, signed word production activated parietal regions that were not activated by spoken word production. Posterior superior temporal gyrus was activated earliest and to the greatest extent during auditory word repetition, and the basal temporal-occipital cortex was activated similarly during naming and reading, reflecting the different modalities of input processing. With few exceptions, topographic patterns of ECoG gamma were consistent with ECS maps of the same or similar language tasks. Conclusions: Spoken and signed word production activated many of the same cortical regions, particularly those processing auditory and visual inputs; however, they activated different regions of sensorimotor cortex, and signing activated parietal cortex more than did speech. This study illustrates the utility of electrocorticographic gamma for studying the neuroanatomy and processing dynamics of human language.

Shifts in Gamma Phase–Amplitude Coupling Frequency from Theta to Alpha Over Posterior Cortex During Visual Tasks

The phase of ongoing theta (4–8 Hz) and alpha (8–12 Hz) electrophysiological oscillations is coupled to high gamma (80–150 Hz) amplitude, which suggests that low-frequency oscillations modulate local cortical activity. While this phase–amplitude coupling (PAC) has been demonstrated in a variety of tasks and cortical regions, it has not been shown whether task demands differentially affect the regional distribution of the preferred low-frequency coupling to high gamma. To address this issue we investigated multiple-rhythm theta/alpha to high gamma PAC in two subjects with implanted subdural electrocorticographic grids. We show that high gamma amplitude couples to the theta and alpha troughs and demonstrate that, during visual tasks, alpha/high gamma coupling preferentially increases in visual cortical regions. These results suggest that low-frequency phase to high-frequency amplitude coupling is modulated by behavioral task and may reflect a mechanism for selection between communicating neuronal networks.

High-frequency gamma activity (80-150 Hz) is increased in human cortex during selective attention

OBJECTIVE To study the role of gamma oscillations (>30Hz) in selective attention using subdural electrocorticography (ECoG) in humans. METHODS We recorded ECoG in human subjects implanted with subdural electrodes for epilepsy surgery. Sequences of auditory tones and tactile vibrations of 800 ms duration were presented asynchronously, and subjects were asked to selectively attend to one of the two stimulus modalities in order to detect an amplitude increase at 400 ms in some of the stimuli. RESULTS Event-related ECoG gamma activity was greater over auditory cortex when subjects attended auditory stimuli and was greater over somatosensory cortex when subjects attended vibrotactile stimuli. Furthermore, gamma activity was also observed over prefrontal cortex when stimuli appeared in either modality, but only when they were attended. Attentional modulation of gamma power began approximately 400 ms after stimulus onset, consistent with the temporal demands on attention. The increase in gamma activity was greatest at frequencies between 80 and 150 Hz, in the so-called high-gamma frequency range. CONCLUSIONS There appears to be a strong link between activity in the high-gamma range (80-150 Hz) and selective attention. SIGNIFICANCE Selective attention is correlated with increased activity in a frequency range that is significantly higher than what has been reported previously using EEG recordings.

Optimizing parameters for terminating cortical afterdischarges with pulse stimulation.

Summary:  Purpose: We previously reported that brief pulses of electrical stimulation (BPSs) can terminate afterdischarges (ADs) during cortical stimulation. We investigated conditions under which BPS is more likely to suppress ADs.

Redefining the role of Broca’s area in speech

Significance Broca’s area is widely recognized to be important for speech production, but its specific role in the dynamics of cortical language networks is largely unknown. Using direct cortical recordings of these dynamics during vocal repetition of written and spoken words, we found that Broca’s area mediates a cascade of activation from sensory representations of words in temporal cortex to their corresponding articulatory gestures in motor cortex, but it is surprisingly quiescent during articulation. Contrary to classic notions of this area’s role in speech, our results indicate that Broca’s area does not participate in production of individual words, but coordinates the transformation of information processing across large-scale cortical networks involved in spoken word production, prior to articulation. For over a century neuroscientists have debated the dynamics by which human cortical language networks allow words to be spoken. Although it is widely accepted that Broca’s area in the left inferior frontal gyrus plays an important role in this process, it was not possible, until recently, to detail the timing of its recruitment relative to other language areas, nor how it interacts with these areas during word production. Using direct cortical surface recordings in neurosurgical patients, we studied the evolution of activity in cortical neuronal populations, as well as the Granger causal interactions between them. We found that, during the cued production of words, a temporal cascade of neural activity proceeds from sensory representations of words in temporal cortex to their corresponding articulatory gestures in motor cortex. Broca’s area mediates this cascade through reciprocal interactions with temporal and frontal motor regions. Contrary to classic notions of the role of Broca’s area in speech, while motor cortex is activated during spoken responses, Broca’s area is surprisingly silent. Moreover, when novel strings of articulatory gestures must be produced in response to nonword stimuli, neural activity is enhanced in Broca’s area, but not in motor cortex. These unique data provide evidence that Broca’s area coordinates the transformation of information across large-scale cortical networks involved in spoken word production. In this role, Broca’s area formulates an appropriate articulatory code to be implemented by motor cortex.

Single-Trial Speech Suppression of Auditory Cortex Activity in Humans

The human auditory cortex is engaged in monitoring the speech of interlocutors as well as self-generated speech. During vocalization, auditory cortex activity is reported to be suppressed, an effect often attributed to the influence of an efference copy from motor cortex. Single-unit studies in non-human primates have demonstrated a rich dynamic range of single-trial auditory responses to self-speech consisting of suppressed, nonsuppressed and excited auditory neurons. However, human research using noninvasive methods has only reported suppression of averaged auditory cortex responses to self-generated speech. We addressed this discrepancy by recording electrocorticographic activity from neurosurgical subjects performing auditory repetition tasks. We observed that the degree of suppression varied across different regions of auditory cortex, revealing a variety of suppressed and nonsuppressed responses during vocalization. Importantly, single-trial high-gamma power (γHigh, 70–150 Hz) robustly tracked individual auditory events and exhibited stable responses across trials for suppressed and nonsuppressed regions.

Electrocorticographic amplitude predicts finger positions during slow grasping motions of the hand

Four human subjects undergoing subdural electrocorticography for epilepsy surgery engaged in a range of finger and hand movements. We observed that the amplitudes of the low-pass filtered electrocorticogram (ECoG), also known as the local motor potential (LMP), over specific peri-Rolandic electrodes were correlated (p < 0.001) with the position of individual fingers as the subjects engaged in slow and deliberate grasping motions. A generalized linear model (GLM) of the LMP amplitudes from those electrodes yielded predictions for positions of the fingers that had a strong congruence with the actual finger positions (correlation coefficient, r; median = 0.51, maximum = 0.91), during displacements of up to 10 cm at the fingertips. For all the subjects, decoding filters trained on data from any given session were remarkably robust in their prediction performance across multiple sessions and days, and were invariant with respect to changes in wrist angle, elbow flexion and hand placement across these sessions (median r = 0.52, maximum r = 0.86). Furthermore, a reasonable prediction accuracy for grasp aperture was achievable with as few as three electrodes in all subjects (median r = 0.49; maximum r = 0.90). These results provide further evidence for the feasibility of robust and practical ECoG-based control of finger movements in upper extremity prosthetics.