Local field potentials reflect cortical population dynamics in a region-specific and frequency-dependent manner

Gallego-Carracedo, Cecilia; Chowdhury, Raeed H.; Miller, Lee E.; Gallego, Juan Álvaro

doi:10.7554/elife.73155

Cited by 37 publications

(34 citation statements)

References 106 publications

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“…High-frequency activity. High-gamma activity (120 to 200 Hz; HFA) has been closely linked with multi-unit activity (Gallego-Carracedo et al, 2022;Leszczynski et al, 2020;Ray & Maunsell, 2011;Rich & Wallis, 2017) and was therefore used as a surrogate marker of population activity. Note that our frequency range for HFA is higher compared to previous studies (~80-150 Hz; c.f., Canolty et al, 2006;Ray & Maunsell, 2011;Rich & Wallis, 2017) to minimize a potential overlap with the ripple frequency band (80 to 120 Hz).…”

Section: Methodsmentioning

confidence: 99%

“…A testable hypothesis arising from our observations is that SW-R should trigger state transitions in both the PFC and MTL to optimize inter-areal information reactivation and transfer. Here, we estimated high-frequency activity (120-200 Hz; HFA) as a surrogate marker of multi-unit population activity (Gallego-Carracedo et al, 2022;Leszczynski et al, 2020;Ray & Maunsell, 2011;Rich & Wallis, 2017). Note that we excluded the human ripple-band (80-120 Hz) from our HFA definition to avoid confounded estimates (SI Appendix, Fig.…”

Section: Mtl and Pfc Sw-r Differentially Shape Population Activitymentioning

confidence: 99%

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An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

Schalkwijk

Weber

Hahn

et al. 2022

Preprint

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The hippocampal sharp-wave ripple (SW-R) is the key substrate of the hippocampal-neocortical dialogue underlying memory formation. Recently, it became evident that SW-R are not unique to archicortex, but constitute a wide-spread neocortical phenomenon. To date, little is known about morphological and functional similarities between archi- and neocortical SW-R. Leveraging intracranial recordings from the human hippocampus and prefrontal cortex during sleep, our results reveal region-specific functional specializations, albeit a near-uniform morphology. While hippocampal SW-R trigger directional hippocampal-to-neocortical information flow, neocortical SW-R reduce information flow to minimize interference. At the population level, hippocampal SW-R confined population dynamics to a low-dimensional subspace, while neocortical SW-R diversified the population response; functionally uncoupling the hippocampal-neocortical network. Critically, our replication in rodents demonstrated the same division-of-labor between archi-and neocortical SW-R. These results uncover an evolutionary preserved mechanism where coordinated interplay between hippocampal and neocortical SW-R temporally segregates hippocampal information transfer from neocortical processing.

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Section: Methodsmentioning

confidence: 99%

Section: Mtl and Pfc Sw-r Differentially Shape Population Activitymentioning

confidence: 99%

An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

Schalkwijk

Weber

Hahn

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Spiking information is difficult to obtain in this population, and surface electrode arrays and depth electrodes provide opportunities to record neural activity across large spatial scales. Alternatively, H γ has been shown to be correlated with underlying latent spiking dynamics( 59 ). It remains to be seen how L γ -H γ PAC may relate to the latent spiking dynamics.…”

Section: Discussionmentioning

confidence: 99%

High-gamma activity is coupled to low-gamma oscillations in precentral cortices and modulates with movement and speech

Nie

Flint²,

Prakash³

et al. 2023

Preprint

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Planning and executing motor behaviors requires coordinated neural activity among multiple cortical and subcortical regions of the brain. Phase-amplitude coupling between the high-gamma band amplitude and the phase of low frequency oscillations (theta, alpha, beta) has been proposed to reflect neural communication, as has synchronization of low-gamma oscillations. However, coupling between low-gamma and high-gamma bands has not been investigated. Here, we measured phase-amplitude coupling between low- and high-gamma in monkeys performing a reaching task and in humans either performing finger movements or speaking words aloud. We found significant coupling between low-gamma phase and high-gamma amplitude in multiple sensorimotor and premotor cortices of both species during all tasks. This coupling modulated with the onset of movement. These findings suggest that interactions between the low and high gamma bands are markers of network dynamics related to movement and speech generation.

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“…If DOI is indeed disrupting rest-related synchronization within cortex, we predicted that we would see a disruption of that characteristic relationship. To examine this possibility we performed latent dynamical canonical correlation analysis (CCA) [44]. Latent dynamical CCA analysis takes advantage of ongoing neural data and is well-suited for examining the relationship between LFP power and spiking over longer periods of time, unlike phase locking analyses which are better suited for event-centered, trialized data during stereotyped behaviors.…”

Section: Doi Disrupts the Characteristic Relationship Between Lfp And...mentioning

confidence: 99%

The classic psychedelic DOI induces a persistent desynchronized state in medial prefrontal cortex

Olson

Bartlett

Sonneborn

et al. 2023

Preprint

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Administration or consumption of classic psychedelics (CPs) leads to profound changes in experience which are often described as highly novel and meaningful. They have shown substantial promise in treating depressive symptoms and may be therapeutic in other situations. Although research suggests that the therapeutic response is correlated with the intensity of the experience, the neural circuit basis for the alterations in experience caused by CPs requires further study. The medial prefrontal cortex (mPFC), where CPs have been shown to induce rapid, 5-HT2A receptor-dependent structural and neurophysiological changes, is believed to be a key site of action. To investigate the acute neural circuit changes induced by CPs, we recorded single neurons and local field potentials in the mPFC of freely behaving mice after administration of the 5-HT2A/2C receptor-selective CP, 2,5-Dimethoxy-4-iodoamphetamine (DOI). We segregated recordings into active and rest periods in order to examine cortical activity during desynchronized (active) and synchronized (rest) states. We found that DOI induced a robust decrease in low frequency power and decoupled rhythmic activity from neural population dynamics when animals were at rest, attenuating the usual synchronization that occurs during less active behavioral states. DOI also increased broadband gamma power and suppressed activity in fast-spiking neurons in both active and rest periods. Together, these results show that the CP DOI induces persistent desynchronization in mPFC, including during rest when mPFC typically exhibits more synchronized activity. This shift in cortical dynamics may in part underlie the longer-lasting effects of CPs on plasticity, and may be critical to their therapeutic properties.

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Local field potentials reflect cortical population dynamics in a region-specific and frequency-dependent manner

Cited by 37 publications

References 106 publications

An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

High-gamma activity is coupled to low-gamma oscillations in precentral cortices and modulates with movement and speech

The classic psychedelic DOI induces a persistent desynchronized state in medial prefrontal cortex

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