•During visual naming, high-gamma modulation occurs in a posteroanterior sequential pattern with overlapping temporal profiles.•Cortical activations during visual naming represent cognitive ...sub-components with different relative contributions from the left and right cerebral hemispheres.•Post-surgical neuropsychological deficits correlated with the location of resected parcels within the visual naming network.
Cerebral spatiotemporal dynamics of visual naming were investigated in epilepsy patients undergoing stereo-electroencephalography (SEEG) monitoring.
Brain networks were defined by Parcel-Activation-Resection-Symptom matching (PARS) approach by matching high-gamma (50–150 Hz) modulations (HGM) in neuroanatomic parcels during visual naming, with neuropsychological outcomes after resection/ablation of those parcels. Brain parcels with >50% electrode contacts simultaneously showing significant HGM were aligned, to delineate spatiotemporal course of naming-related HGM.
In 41 epilepsy patients, neuroanatomic parcels showed sequential yet temporally overlapping HGM course during visual naming. From bilateral occipital lobes, HGM became increasingly left lateralized, coursing through limbic system. Bilateral superior temporal HGM was noted around response time, and right frontal HGM thereafter. Correlations between resected/ablated parcels, and post-surgical neuropsychological outcomes showed specific regional groupings.
Convergence of data from spatiotemporal course of HGM during visual naming, and functional role of specific parcels inferred from neuropsychological deficits after resection/ablation of those parcels, support a model with six cognitive subcomponents of visual naming having overlapping temporal profiles.
Cerebral substrates supporting visual naming are bilaterally distributed with relative hemispheric contribution dependent on cognitive demands at a specific time. PARS approach can be extended to study other cognitive and functional brain networks.
Improvement in visual naming abilities throughout the childhood and adolescence supports development of higher-order linguistic skills. We investigated neuronal circuits underlying improvement in the ...speed of visual naming with age, and age-related dynamics of these circuits.
Response times were electronically measured during an overt visual naming task in epilepsy patients undergoing stereo-EEG monitoring. Coherence modulations among pairs of neuroanatomic parcels were computed and analyzed for relationship with response time and age.
During the overt visual naming task, mean response time (latency) significantly decreased from 4 to 23 years of age. Coherence modulations during visual naming showed that increased connectivity between certain brain regions, particularly that between left fusiform gyrus/left parahippocampal gyrus and left frontal operculum, is associated with improvement in naming speed. Also, decreased connectivity in other brain regions, particularly between left angular and supramarginal gyri, is associated with decreased mean response time. Further, coherence modulations between left frontal operculum and both left fusiform and left posterior cingulate gyri significantly increase, while that between left angular and supramarginal gyri significantly decrease, with age.
Naming speed continues to improve from pre-school years into young adulthood. This age-related improvement in efficiency of naming environmental objects occurs likely because of strengthened direct connectivity between semantic and phonological nodes, and elimination of intermediate higher-order cognitive steps.
We prospectively validated stereo-electroencephalography (EEG) electrical stimulation mapping (ESM) of language against a reference standard of meta-analytic functional magnetic resonance imaging ...(fMRI) framework (Neurosynth).
Language ESM was performed using 50 Hz, biphasic, bipolar, stimulation at 1–8 mA, with a picture naming task. Electrode contacts (ECs) were scored as ESM+ if ESM interfered with speech/language function. For each patient, presurgical MRI was transformed to a standard space and coregistered with computed tomographic (CT) scan to obtain EC locations. After whole-brain parcellation, this fused image data were intersected with three-dimensional language fMRI (Neurosynth), and each EC was classified as lying within/outside the fMRI language parcel. Diagnostic odds ratio (DOR) and other indices were estimated. Current thresholds for language inhibition and after-discharges (ADs) were analyzed using multivariable linear mixed models.
In 10 patients (5 females), aged 5.4–21.2 years, speech/language inhibition was noted with ESM on 87/304 (29%) ECs. Stereo-EEG language ESM was a valid classifier of fMRI (Neurosynth) language sites (DOR: 9.02, p < 0.0001), with high specificity (0.87) but poor sensitivity (0.57). Similar diagnostic indices were seen for ECs in frontal or posterior regions, and gray or white matter.
Language threshold (3.1 ± 1.5 mA) was lower than AD threshold (4.0 ± 2.0 mA, p = 0.0001). Language and AD thresholds decreased with age and intelligence quotient. Electrical stimulation mapping triggered seizures/auras represented patients' habitual semiology with 1 Hz stimulation.
Stereo-EEG ESM can reliably identify cerebral parcels with/without language function but may under detect all language sites. We suggest a 50-Hz stimulation protocol for language ESM with stereo-EEG.
•We validated electrical stimulation mapping with stereo-EEG for localization of language functional neuroanatomy•Stereo-EEG electrical stimulation classified language sites (diagnostic odds ratio 9.0) with high specificity (0.87)•We suggest 50 Hz stimulation for language localization and 1 Hz stimulation for attempt to reproduce habitual seizures
•Stimulation within auditory cortex produced facial expressions and perioral motor responses in approximately one-third of patients.•Cortical sites with motor and language responses within transverse ...temporal gyrus and adjacent cortex (TGG+) showed different yet overlapping neurophysiologic characteristics.•TTG+ likely participates in non-verbal responses to low-level auditory and/or emotional cues during a communicative discourse.
We investigated the role of transverse temporal gyrus and adjacent cortex (TTG+) in facial expressions and perioral movements.
In 31 patients undergoing stereo-electroencephalography monitoring, we describe behavioral responses elicited by electrical stimulation within the TTG+. Task-induced high-gamma modulation (HGM), auditory evoked responses, and resting-state connectivity were used to investigate the cortical sites having different types of responses on electrical stimulation.
Changes in facial expressions and perioral movements were elicited on electrical stimulation within TTG+ in 9 (29%) and 10 (32%) patients, respectively, in addition to the more common language responses (naming interruptions, auditory hallucinations, paraphasic errors). All functional sites showed auditory task induced HGM and evoked responses validating their location within the auditory cortex, however, motor sites showed lower peak amplitudes and longer peak latencies compared to language sites. Significant first-degree connections for motor sites included precentral, anterior cingulate, parahippocampal, and anterior insular gyri, whereas those for language sites included posterior superior temporal, posterior middle temporal, inferior frontal, supramarginal, and angular gyri.
Multimodal data suggests that TTG+ may participate in auditory-motor integration.
TTG+ likely participates in facial expressions in response to emotional cues during an auditory discourse.
•Stereo-EEG sensorimotor mapping was prospectively compared with reference neuroanatomy.•Electrical stimulation mapping localized anatomic sensorimotor parcels with high accuracy.•Sensorimotor ...thresholds below after-discharge thresholds suggest safety of stereo-EEG ESM.
We evaluated stereo-EEG electrical stimulation mapping (ESM) for localization of anatomic sensorimotor parcels in pediatric patients with drug-resistant epilepsy. We also analyzed sensorimotor and after-discharge thresholds, and the somatotopy of sensorimotor responses.
ESM was performed with 50 Hz, biphasic, 2–3 s trains, using 1–9 mA current. Pre- and post-implant neuroimaging was co-registered and intersected with Neurosynth reference, to classify each electrode contact as lying within/outside an anatomic sensorimotor parcel. Indices of diagnostic performance were computed. Sensorimotor and after-discharge thresholds were analyzed using multivariable linear mixed models.
In 15 patients (6 females), aged 5.5–21.2 years, ESM showed high accuracy (0.80), high specificity (0.86), and diagnostic odds ratio (11.4, p < 0.0001) for localization of sensorimotor parcels. Mean sensorimotor threshold (3.4 mA) was below mean after-discharge threshold (4.2 mA, p = 0.0004). Sensorimotor and after-discharge thresholds showed a significant decrease with increasing intelligence quotient. Somatotopy of sensorimotor responses was mapped to standardized brain parcels.
We provide evidence for diagnostic validity and safety of stereo-EEG sensorimotor ESM.
The somatotopy of sensorimotor responses elicited with electrical stimulation provide new insights into mechanisms of motor control and sensory perception.
•An approach for analysis of task-related high-gamma modulation in stereo-EEG using distribution of power differential clusters is described.•Stereo-EEG high-gamma language mapping effectively ...localized reference neuroanatomy (Neurosynth).•Stereo-EEG high-gamma language mapping also adequately classified electrical stimulation mapping speech/language sites.
A novel analytic approach for task-related high-gamma modulation (HGM) in stereo-electroencephalography (SEEG) was developed and evaluated for language mapping.
SEEG signals, acquired from drug-resistant epilepsy patients during a visual naming task, were analyzed to find clusters of 50–150 Hz power modulations in time–frequency domain. Classifier models to identify electrode contacts within the reference neuroanatomy and electrical stimulation mapping (ESM) speech/language sites were developed and validated.
In 21 patients (9 females), aged 4.8–21.2 years, SEEG HGM model predicted electrode locations within Neurosynth language parcels with high diagnostic odds ratio (DOR 10.9, p < 0.0001), high specificity (0.85), and fair sensitivity (0.66). Another SEEG HGM model classified ESM speech/language sites with significant DOR (5.0, p < 0.0001), high specificity (0.74), but insufficient sensitivity. Time to largest power change reliably localized electrodes within Neurosynth language parcels, while, time to center-of-mass power change identified ESM sites.
SEEG HGM mapping can accurately localize neuroanatomic and ESM language sites.
Predictive modelling incorporating time, frequency, and magnitude of power change is a useful methodology for task-related HGM, which offers insights into discrepancies between HGM language maps and neuroanatomy or ESM.
•Intracranial high-frequency oscillations (HFOs) show a significant diurnal rhythm.•Diurnal rhythm of HFOs is relatively attenuated within the seizure-onset zone (SOZ).•Peak difference in HFO density ...within/outside SOZ consistently precedes seizures.•Difference in HFO density within/outside SOZ peaks at 1st hour after arousal and ±2 hours around sleep onset.
Seizures are known to occur with diurnal and other rhythms. To gain insight into the neurophysiology of periodicity of seizures, we tested the hypothesis that intracranial high-frequency oscillations (HFOs) show diurnal rhythms and sleep-wake cycle variation. We further hypothesized that HFOs have different rhythms within and outside the seizure-onset zone (SOZ).
In drug-resistant epilepsy patients undergoing stereotactic-EEG (SEEG) monitoring to localize SOZ, we analyzed the number of 50-200 Hz HFOs/channel/minute (HFO density) through a 24-hour period. The distribution of HFO density during the 24-hour period as a function of the clock time was analyzed with cosinor model, and for non-uniformity with the sleep-wake cycle.
HFO density showed a significant diurnal rhythm overall and both within and outside SOZ. This diurnal rhythm of HFO density showed significantly lower amplitude and longer acrophase within SOZ compared to outside SOZ. The peaks of difference in HFO density within and outside SOZ preceded the seizures by approximately 4 hours. The difference in HFO density within and outside SOZ also showed a non-uniform distribution as a function of sleep-wake cycle, with peaks at first hour after arousal and ±2 hours around sleep onset.
Our study shows that the diurnal rhythm of intracranial HFOs is more robust outside the SOZ. This suggests cortical tissue within SOZ generates HFOs relatively more uniformly throughout the day with attenuation of expected diurnal rhythm. The difference in HFO density within and outside SOZ also showed non-uniform distribution according to clock times and the sleep-wake cycle, which can be a potential biomarker for preferential times of pathological cortical excitability. A temporal correlation with seizure occurrence further substantiates this hypothesis.
Summary
Objective
We studied age‐related dynamics of information sharing among cortical language regions with electrocorticographic high‐gamma modulation during picture‐naming and story‐listening ...tasks.
Methods
Seventeen epilepsy patients aged 4‐19 years, undergoing extraoperative monitoring with left‐hemispheric subdural electrodes, were included. Mutual information (MI), a nondirectional measure of shared information, between 16 pairs of cortical regions of interest, was computed from trial‐averaged 70–150 Hz power modulations during language tasks. Impact of age on pairwise MI between language regions and their determinants were ascertained with regression analysis.
Results
During picture naming, significant increase in MI with age was seen between pairwise combinations of Broca's area, inferior precentral gyrus (iPreC), and frontal association cortex (FAC); Wernicke's area and posterior association cortex (PAC); and Broca's and Wernicke's areas. During story listening, significant age‐related increase in MI was seen between Wernicke's area and either Broca's area, FAC, or PAC; and between Broca's area and FAC. Significant impact of baseline intelligence quotient was seen on the relationship between age and MI for all pairs, except between Broca's area and iPreC. The mean MI was higher during naming compared to listening for pairs including iPreC with Broca's area, FAC, or PAC and was lower for pairs of Wernicke's area or PAC with anterior language regions.
Significance
Information sharing matures with age “within” frontal and temporoparietal language cortices, and “between” Broca's and Wernicke's areas. This study provides evidence for distinct patterns of developmental plasticity within perisylvian language cortex and has implications for planning epilepsy surgery.
