Frequency Selectivity of Persistent Cortical Oscillatory Responses to Auditory Rhythmic Stimulation.

Cortical oscillations have been proposed to play a functional role in speech and music perception, attentional selection, and working memory, via the mechanism of neural entrainment. One of the properties of neural entrainment that is often taken for granted is that its modulatory effect on ongoing oscillations outlasts rhythmic stimulation. We tested the existence of this phenomenon by studying cortical neural oscillations during and after presentation of melodic stimuli in a passive perception paradigm. Melodies were composed of ∼60 and ∼80 Hz tones embedded in a 2.5 Hz stream. Using intracranial and surface recordings in male and female humans, we reveal persistent oscillatory activity in the high-γ band in response to the tones throughout the cortex, well beyond auditory regions. By contrast, in response to the 2.5 Hz stream, no persistent activity in any frequency band was observed. We further show that our data are well captured by a model of damped harmonic oscillator and can be classified into three classes of neural dynamics, with distinct damping properties and eigenfrequencies. This model provides a mechanistic and quantitative explanation of the frequency selectivity of auditory neural entrainment in the human cortex.SIGNIFICANCE STATEMENT It has been proposed that the functional role of cortical oscillations is subtended by a mechanism of entrainment, the synchronization in phase or amplitude of neural oscillations to a periodic stimulation. One of the properties of neural entrainment that is often taken for granted is that its modulatory effect on ongoing oscillations outlasts rhythmic stimulation. Using intracranial and surface recordings of humans passively listening to rhythmic auditory stimuli, we reveal consistent oscillatory responses throughout the cortex, with persistent activity of high-γ oscillations. On the contrary, neural oscillations do not outlast low-frequency acoustic dynamics. We interpret our results as reflecting harmonic oscillator properties, a model ubiquitous in physics but rarely used in neuroscience.

The Ictal Signature of Thalamus and Basal Ganglia in Focal Epilepsy: A SEEG Study.

OBJECTIVE: To determine the involvement of subcortical regions in human epilepsy by analyzing direct recordings from these regions during epileptic seizures using stereo-EEG (SEEG). METHODS: We studied the SEEG recordings of a large series of patients (74 patients, 157 seizures) with an electrode sampling the thalamus and in some cases also the basal ganglia (caudate nucleus, 22 patients; and putamen, 4 patients). We applied visual analysis and signal quantification methods (Epileptogenicity Index [EI]) to their ictal recordings and compared electrophysiologic with clinical data. RESULTS: We found that in 86% of patients, thalamus was involved during seizures (visual analysis) and 20% showed high values of epileptogenicity (EI >0.3). Basal ganglia may also disclose high values of epileptogenicity (9% in caudate nucleus) but to a lesser degree than thalamus (p < 0.01). We observed different seizure onset patterns including low voltage high frequency activities. We found high values of thalamic epileptogenicity in different epilepsy localizations, including opercular and motor epilepsies. We found no difference between epilepsy etiologies (cryptogenic vs malformation of cortical development, p = 0.77). Thalamic epileptogenicity was correlated with the extension of epileptogenic networks (p = 0.02, ρ 0.32). We found a significant effect (p < 0.05) of thalamic epileptogenicity regarding the postsurgical outcome (higher thalamic EI corresponding to higher probability of surgical failure). CONCLUSIONS: Thalamic involvement during seizures is common in different seizure types. The degree of thalamic epileptogenicity is a possible marker of the epileptogenic network extension and of postsurgical prognosis.

Asymmetric sampling in human auditory cortex reveals spectral processing hierarchy.

Speech perception is mediated by both left and right auditory cortices but with differential sensitivity to specific acoustic information contained in the speech signal. A detailed description of this functional asymmetry is missing, and the underlying models are widely debated. We analyzed cortical responses from 96 epilepsy patients with electrode implantation in left or right primary, secondary, and/or association auditory cortex (AAC). We presented short acoustic transients to noninvasively estimate the dynamical properties of multiple functional regions along the auditory cortical hierarchy. We show remarkably similar bimodal spectral response profiles in left and right primary and secondary regions, with evoked activity composed of dynamics in the theta (around 4-8 Hz) and beta-gamma (around 15-40 Hz) ranges. Beyond these first cortical levels of auditory processing, a hemispheric asymmetry emerged, with delta and beta band (3/15 Hz) responsivity prevailing in the right hemisphere and theta and gamma band (6/40 Hz) activity prevailing in the left. This asymmetry is also present during syllables presentation, but the evoked responses in AAC are more heterogeneous, with the co-occurrence of alpha (around 10 Hz) and gamma (>25 Hz) activity bilaterally. These intracranial data provide a more fine-grained and nuanced characterization of cortical auditory processing in the 2 hemispheres, shedding light on the neural dynamics that potentially shape auditory and speech processing at different levels of the cortical hierarchy.

The effect of medial pulvinar stimulation on temporal lobe seizures.

We investigated the effect of electrical stimulation of the medial pulvinar (PuM) in terms of its effect on temporal lobe seizures. Eight patients with drug-resistant temporal lobe epilepsy undergoing stereoelectroencephalographic exploration were included. All had at least one electrode exploring the PuM. High-frequency (50 Hz) stimulations of the PuM were well tolerated in the majority of them. During diagnostic stimulation to confirm the epileptogenic zone, 19 seizures were triggered by stimulating the hippocampus. During some of these seizures, ipsilateral pulvinar stimulation was applied (130 Hz, pulse width = 450 microseconds, duration = 3-7 seconds, 1-2 mA). Compared to non-PuM-stimulated seizures, five of eight patients experienced clinically less severe seizures, particularly in terms of degree of alteration of consciousness. On the electrical level, seizures were more rapidly clonic with a shorter tonic phase. This proof of concept study is the first to suggest that PuM stimulation could be a well-tolerated and effective means of therapeutic deep brain stimulation in drug-resistant epilepsies.

Temporal envelope processing in the human left and right auditory cortices.

The goal of this study was to determine the temporal response properties of different auditory cortical areas in humans. This is achieved by recording the phase-locked neural activity to white noises modulated sinusoidally in amplitude (AM) at frequencies between 4 and 128 Hz, in the left and right cortices of 20 subjects. Phase-locked neural responses are recorded in four auditory cortical areas with intracerebral electrodes, and modulation transfer functions (MTFs) are computed from these responses. A number of MTFs are bandpass in shape, demonstrating a selective encoding of AM frequencies below 64 Hz in the auditory cortex. This result provides strong physiological support to the idea that the human auditory system decomposes the temporal envelope of sounds (such as speech) into its constituting AM components. Moreover, the results show a predominant response of cortical auditory areas to the lowest AM frequencies (4-16 Hz). This range matches the range of AM frequencies crucial for speech intelligibility, emphasizing therefore the role played by these initial stations of cortical processing in the analysis of speech. Finally, the results show differences in AM sensitivity across cortical areas and hemispheres, and provide a physiological foundation for claims of functional specialization of auditory areas based on previous population measures.