The analysis of cross-frequency coupling (CFC) has become popular in studies involving intracranial and scalp EEG recordings in humans. It has been argued that some cases where CFC is mathematically present may not reflect an interaction of two distinct yet functionally coupled neural sources with different frequencies. Here we provide two empirical examples from intracranial recordings where CFC can be shown to be driven by the shape of a periodic waveform rather than by a functional interaction between distinct sources. Using simulations, we also present a generalized and realistic scenario where such coupling may arise. This scenario, which we term waveform-dependent CFC, arises when sharp waveforms (e.g., cortical potentials) occur throughout parts of the data, in particular if they occur rhythmically. Since the waveforms contain both low- and high-frequency components, these components can be inherently phase-aligned as long as the waveforms are spaced with appropriate intervals. We submit that such behavior of the data, which seems to be present in various cortical signals, cannot be interpreted as reflecting functional modulation between distinct neural sources without additional evidence. In addition, we show that even low amplitude periodic potentials that cannot be readily observed or controlled for, are sufficient for significant CFC to occur.
Research into visual neural activity has focused almost exclusively on onset- or change-driven responses and little is known about how information is encoded in the brain during sustained periods of visual perception. We used intracranial recordings in humans to determine the degree to which the presence of a visual stimulus is persistently encoded by neural activity. The correspondence between stimulus duration and neural response duration was strongest in early visual cortex and gradually diminished along the visual hierarchy, such that is was weakest in inferior-temporal category-selective regions. A similar posterior-anterior gradient was found within inferior temporal face-selective regions, with posterior but not anterior sites showing persistent face-selective activity. The results suggest that regions that appear uniform in terms of their category selectivity are dissociated by how they temporally represent a stimulus in support of ongoing visual perception, and delineate a large-scale organizing principle of the ventral visual stream.
Much of what is known about the timing of visual processing in the brain is inferred from intracranial studies in monkeys, with human data limited to mainly non-invasive methods with lower spatial resolution. Here, we estimated visual onset latencies from electrocorticographic (ECoG) recordings in a patient who was implanted with 112 sub-dural electrodes, distributed across the posterior cortex of the right hemisphere, for pre-surgical evaluation of intractable epilepsy. Functional MRI prior to surgery was used to determine boundaries of visual areas. The patient was presented with images of objects from several categories. Event Related Potentials (ERPs) were calculated across all categories excluding targets, and statistically reliable onset latencies were determined using a bootstrapping procedure over the single trial baseline activity in individual electrodes. The distribution of onset latencies broadly reflected the known hierarchy of visual areas, with the earliest cortical responses in primary visual cortex, and higher areas showing later responses. A clear exception to this pattern was robust, statistically reliable and spatially localized, very early responses on the bank of the posterior intra-parietal sulcus (IPS). The response in the IPS started nearly simultaneously with responses detected in peristriate visual areas, around 60 milliseconds post-stimulus onset. Our results support the notion of early visual processing in the posterior parietal lobe, not respecting traditional hierarchies, and give direct evidence for onset times of visual responses across the human cortex.
The analysis of cross-frequency coupling (CFC) has become popular in studies involving intracranial and scalp EEG recordings in humans. It has been argued that some cases where CFC is mathematically present may not reflect an interaction of two distinct yet functionally coupled neural sources with different frequencies. Here we provide two empirical examples from intracranial recordings where CFC can be shown to be driven by the shape of a periodic waveform rather than by a functional interaction between distinct sources. Using simulations, we also present a generalized and realistic scenario where such coupling may arise. This scenario, which we term waveform-dependent CFC, arises when sharp waveforms (e.g., cortical potentials) occur in a periodic manner throughout parts of the data. Since the waveforms are repeated periodically, they constitute a slow wave that is inherently phase-aligned with the high-frequency component carried by the same waveforms. We submit that such behavior of the data, which seems to be present in various cortical signals, cannot be interpreted as reflecting functional modulation between distinct neural sources without additional evidence. In addition, we show that even low amplitude periodic potentials that cannot be readily observed or controlled for, are sufficient for significant CFC to occur.
Everyday visual experience contains many brief stationary moments when we continue to be consciously aware our sensory input. However, neural activity is dramatically attenuated shortly after the onset response, and it is unclear how the content of our experience remains stable nevertheless. To characterize the spatiotemporal dynamics of object representation in sustained viewing conditions, we use intracranial recordings from ten patients viewing images from variable categories in multiple durations. We reveal that the distributed neural representation of categories and exemplars in posterior-sensory regions remains sustained and stable, mirroring the stability of experience, despite substantial variability in activity after the onset response. Additionally, we find transient coding of visual content in frontoparietal cortex, even when no report is required. Together, our results suggest sustained perception is maintained by sensory regions, not by overall activation magnitude but by the position within an "Experience Subspace", and perceptual changes involve frontoparietal regions, regardless of the task. These findings directly inform recent large-scale attempts to test theories of consciousness.
13Neural populations that encode sensory experience should be persistently active for as long as 14 the experience persists. However, research into visual neural activity has focused almost 15 exclusively on onset-driven responses that cannot account for sustained perception. We used 16 intracranial recordings in humans to determine the degree to which the presence of a visual 17 stimulus is persistently encoded by neural activity. The correspondence between stimulus 18 duration and response duration was strongest in early visual cortex and gradually diminished 19 along the visual hierarchy, such that is was weakest in inferior-temporal category-selective 20 regions. A similar posterior-anterior gradient was found within inferior temporal face-selective 21 regions, with posterior but not anterior sites showing persistent face-selective activity. The 22 results suggest that regions that appear uniform in terms of their category selectivity are 23 dissociated by how they temporally represent a stimulus in support of real-time experience, and 24 delineate a large-scale organizing principle of the ventral visual stream. 25 26 Keywords: Electrocorticography, visual Cortex, sustained perception, high-frequency 27 activity, early visual cortex, inferior temporal cortex, fusiform face area. 28 29 30 crucial for isolating the part of the response driven specifically by the stimulus ongoing 55 presence. However, no duration estimation was required. 56We found that early visual cortex (EVC) high frequency broadband response closely tracked 57 the time course of the stimulus, and this precision decreased along the visual hierarchy, i.e. 58 from V1/V2 to V3/V4, from early visual cortex to inferior temporal (IT) cortex, and from 59 posterior to anterior IT. Only the posterior part of IT robustly encoded the presence of the 60 stimulus over time. This posterior-anterior gradient could not be explained by signal-to-noise 61 ratio or by differential influences of attention or saccade-related activity. 62 63 3 64 Figure 1: Experimental paradigm. (A) Images were presented for 300, 900, or 1500 ms (for 3 subjects 65 also 600 or 1200 ms) with variable inter-stimulus interval (ISI) during which a fixation cross was 66presented. Subjects responded with a button press to presentation of targets (clothing images; 10% of 67 trials). (B) Dual-task control. This task was identical to the first except that subjects also had to respond 68 to rare blurring of the image in the last 200 ms of its presentation. 70Results 71Subjects viewed grayscale images of faces, objects, or other miscellaneous images presented 72 for a duration of 300, 600, 900, 1200 or 1500 milliseconds. To maintain attention subjects 73 responded via button press to a rare target category (clothes, Fig. 1A). All subjects detected the 74 targets successfully (mean±SD hit rate 90.4%±8.6%, false alarm rate 1.9%±3.2%). Responses 75 to the rare targets were not included in the following analyses. Stimulus-induced modulation of 76 the ECoG signal was measured as an increase in the...
What are the neurophysiological correlates of sustained visual processing in the scalp EEG signal? In a previous study using intracranial recordings in humans, we found that presentation of visual stimuli for prolonged durations (up to 1.5 seconds) was associated with two kinds of sustained neural activity patterns: a high-frequency broadband (>30 Hz) response that tracked the duration of the stimulus with high precision in early visual cortex (EVC), and with lesser temporal precision in downstream category-selective areas; and a sustained lowfrequency potential shift appearing in a small subset of EVC sites. Using a similar approach of presenting images for variable durations to identify sustained activity, we provide the first comprehensive characterization of the manifestation of sustained visual responses as recorded with EEG. In a series of four experiments, we found that both high-and lowfrequency sustained responses can be detected on the scalp. The high frequency activity could be detected with high signal to noise ratio only in a subset of individual subjects, in whom it was unequivocal and highly localized. The low frequency sustained response was sensitive to the size and position of the stimulus in the visual field. Both response types showed strong lateralization for stimuli on the left vs. right visual field, suggesting a retinotopic visual cortical source. However, different scalp topographies and different modulation by stimulus properties suggest that the two types of sustained responses are likely driven by distinct sources, and reflect different aspects of sustained processing in the visual cortex.
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