Charles E. Schroeder

Extracellular electrophysiological recordings reflect both the organization of neural activity and the geometry through which that activity is sampled. Here, we used biophysical modeling and experimental recordings from the macaque auditory cortex to determine how cortical activity is transformed across neural sources, extracellular signals, and recording geometries. In a biophysically detailed thalamocortical model, four separately instantiated cortical-column conditions spanning graded thalamic recruitment exhibited a graded response hierarchy across local field potential, current-source density, and multiunit activity, despite signal-dependent differences in the contributions of cortical neuronal populations. We then arranged independently simulated cortical columns into controlled spatial configurations and sampled the same underlying sources using virtual linear laminar and Directional and Scalable (DiSc) electrode arrays. The linear geometry primarily represented variation along cortical depth, whereas DiSc additionally represented circumferential variation associated with lateral source organization, demonstrating that recording geometry determines which spatial dimensions of common underlying activity are represented in extracellular measurements. Experimental recordings obtained with the corresponding geometries were consistent with these model-derived predictions: broadband-noise responses exhibited spatial organization shared across tone-evoked responses in both multidimensional DiSc maps and laminar profiles, despite substantial variation in frequency-dependent response magnitude across penetrations. Together, these results show that extracellular measurements represent an interaction between biological source organization and recording geometry. Biophysical forward modeling therefore provides a framework for determining which features of underlying circuit organization remain identifiable after extracellular sampling and for relating neural-interface design to the dimensions of cortical activity accessible experimentally.

Transient high-frequency activity (HFA) in local field potentials exhibits substantial variability across trials and behavioral states, yet its functional role in sensory representation remains poorly understood. Here, we tested whether transient HFA events carry stimulus-related information through their temporal, spectral, and phase-dependent properties. Using intracranial recordings from 21 human participants performing a visual localizer task, we extracted transient HFA events and quantified their features using information-theoretic and decoding analyses. Individual event features carried only modest information about stimulus identity, and response magnitude and morphology-related properties contributed minimally to decoding performance. Instead, decoding was dominated by temporal alignment and low-frequency phase. Critically, representing transient events as distributed low-frequency phase configurations across electrodes substantially improved cross-trial decoding performance, whereas disrupting distributed phase structure eliminated this decoding advantage. These findings indicate that stimulus-related structure in transient HFA does not primarily arise from isolated local event properties, but instead emerges through distributed, phase-dependent network dynamics. More broadly, the results provide a framework for understanding how transient high-frequency neural activity contributes to sensory representations across distributed cortical networks.

The flow of information between cortical regions depends on the excitability at each site, which is reflected in fluctuating field potentials. It remains uncertain how global changes in field potentials affect the latency and strength of cortico-cortical couplings. Therefore, we measured changes in oscillations and inter-regional couplings by recording intracranially from the human cerebral cortex. As participants listened to an auditory narrative, global increases in low-frequency (4-14 Hz) power were associated with stronger and more delayed inter-regional couplings. Conversely, increases in broadband high-frequency power were associated with weaker coupling and zero lag. In network oscillator models, these changes in cortico-cortical latency can be generated by varying the effective influence of inter-regional projections relative to intra-regional dynamics. Altogether, low-frequency oscillations appear to modulate information flow across the human cerebral cortex, as they covary with the timing of peak excitability between regions, and this process may be regulated by nonspecific ascending projections.

Our continuous visual experience in daily life is dominated by change. Previous research has focused on visual change due to stimulus motion, eye movements or unfolding events, but not their combined impact across the brain, or their interactions with semantic novelty. We investigate the neural responses to these sources of novelty during film viewing. We analyzed intracranial recordings in humans across 6328 electrodes from 23 individuals. Responses associated with saccades and film cuts were dominant across the entire brain. Film cuts at semantic event boundaries were particularly effective in the temporal and medial temporal lobe. Saccades to visual targets with high visual novelty were also associated with strong neural responses. Specific locations in higher-order association areas showed selectivity to either high or low-novelty saccades. We conclude that neural activity associated with film cuts and eye movements is widespread across the brain and is modulated by semantic novelty.

The flow of information between cortical regions depends on the excitability at each site, which is reflected in fluctuating field potentials. It remains uncertain how global changes in field potentials affect the latency and strength of cortico-cortical couplings. Therefore, we measured changes in oscillations and inter-regional couplings by recording intracranially from the human cerebral cortex. As participants listened to an auditory narrative, global increases in low-frequency (4-14 Hz) power were associated with stronger and more delayed inter-regional couplings. Conversely, increases in broadband high-frequency power were associated with weaker coupling and zero lag. In network oscillator models, these changes in cortico-cortical latency can be generated by varying the effective influence of inter-regional projections relative to intra-regional dynamics. Altogether, low-frequency oscillations appear to modulate information flow across the human cerebral cortex, as they covary with the timing of peak excitability between regions, and this process may be regulated by nonspecific ascending projections.

Summary: In natural “active” vision, humans and other primates use eye movements (saccades) to sample bits of information from visual scenes. In this process, nonretinal signals linked to saccades shift visual cortical neurons to a high excitability state as each saccade ends. The extent of this saccadic modulation outside of the visual system is unknown. Here, we show that during natural viewing, saccades modulate excitability in numerous auditory cortical areas, with a pattern complementary to that seen in visual areas. Bi-directional functional connectivity patterns suggest that these effects may arise from regions involved in saccade generation. By using saccadic signals to yoke excitability states in auditory areas to those in visual areas, the brain can improve information processing in complex natural settings.

Natural conversation is multisensory: when we can see the speaker's face, visual speech cues improve our comprehension. The neuronal mechanisms underlying this phenomenon remain unclear. The two main alternatives are visually mediated phase modulation of neuronal oscillations (excitability fluctuations) in auditory neurons and visual input-evoked responses in auditory neurons. Investigating this question using naturalistic audiovisual speech with intracranial recordings in humans of both sexes, we find evidence for both mechanisms. Remarkably, auditory cortical neurons track the temporal dynamics of purely visual speech using the phase of their slow oscillations and phase-related modulations in broadband high-frequency activity. Consistent with known perceptual enhancement effects, the visual phase reset amplifies the cortical representation of concomitant auditory speech. In contrast to this, and in line with earlier reports, visual input reduces the amplitude of evoked responses to concomitant auditory input. We interpret the combination of improved phase tracking and reduced response amplitude as evidence for more efficient and reliable stimulus processing in the presence of congruent auditory and visual speech inputs.SIGNIFICANCE STATEMENTWatching the speaker can facilitate our understanding of what is being said. The mechanisms responsible for this influence of visual cues on the processing of speech remain incompletely understood. We studied these mechanisms by recording the electrical activity of the human brain through electrodes implanted surgically inside the brain. We found that visual inputs can operate by directly activating auditory cortical areas, and also indirectly by modulating the strength of cortical responses to auditory input. Our results help to understand the mechanisms by which the brain merges auditory and visual speech into a unitary perception.

BHA (aka high gamma) correlates with neuronal firing, but is generated mainly by dendritic processes separable from firing.