Microscale physiological events on the human cortical surface

Paulk, Angelique C.; Yang, Jimmy C.; Cleary, Daniel R.; Soper, Daniel J.; Halgren, Milan; O’Donnell, Alexandra R.; Lee, Sang‐Heon; Ganji, Mehran; Ro, Yun Goo; Oh, Hongseok; Hossain, Lorraine; Lee, Ji‐Hwan; Tchoe, Youngbin; Rogers, Nicholas; Kılıç, Kıvılcım; Ryu, Sang Baek; Lee, Seung Woo; Hermiz, John; Gilja, Vikash; Ulbert, István; Fabó, Dániel; Devinsky, Orrin; Madsen, Joseph R.; Schomer, Donald L.; Eskandar, Emad N.; Lee, Jong Woo; Maus, Douglas; Devor, Anna; Fried, Shelley I.; Jones, Pamela S.; Nahed, Brian V.; Ben-Haim, Sharona; Bick, Sarah K; Richardson, R. Mark; Raslan, Ahmed M.; Siler, Dominic A.; Cahill, Daniel P.; Williams, Ziv; Cosgrove, G. Rees; Dayeh, Shadi A.; Cash, Sydney S.

doi:10.1101/770743

Cited by 5 publications

(5 citation statements)

References 92 publications

(155 reference statements)

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“…Surface recordings have followed these footsteps and recently enabled recordings from thousands of contacts [3]. In other studies, surface recordings advanced to resolve single unit activity from the surface of the brain in animals and humans [4][5][6]. To investigate the inter-relationship between surface and depth recordings, separate surface and depth electrodes are typically used [7,8].…”

Section: Introductionmentioning

confidence: 99%

Epi-Intra neural probes with glassy carbon microelectrodes help elucidate neural coding and stimulus encoding in 3D volume of tissue

et al. 2020

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Objective. In this study, we demonstrate practical applications of a novel 3-dimensional neural probe for simultaneous electrophysiological recordings from the surface of the brain as well as deep intra-cortical tissue. We used this 3D probe to investigate signal propagation mechanisms between neuronal cells and their responses to stimuli in a 3D fashion. Approach. This novel probe leverage 2D thin-film microfabrication technique to combine an epi-cortical (surface) and an intra-cortical (depth) microelectrode arrays (Epi-Intra), that unfold into an origami 3D-like probe during brain implantation. The flexible epi-cortical component conforms to the brain surface while the intra-cortical array is reinforced with stiffer durimide polymer layer for ease of tissue penetration. The microelectrodes are made of glassy carbon material that is biocompatible and has low electrochemical impedance that is important for high fidelity neuronal recordings. These recordings were performed on the auditory region of anesthetized European starling songbirds during playback of conspecific songs as auditory stimuli. Main results. The Epi-Intra probe recorded broadband activity including local field potentials (LFPs) signals as well as single-unit activity and multi-unit activity from both surface and deep brain. The majority of recorded cellular activities were stimulus-locked and exhibited low noise. Notably, while LFPs recorded on surface and depth electrodes did not exhibit strong correlation, composite receptive fields (CRFs)—extracted from individual neuron cells through a non-linear model and that are cell-dependent—were correlated. Significance. These findings demonstrate that CRFs extracted from Epi-Intra recordings are excellent candidates for neural coding and for understanding the relationship between sensory neuronal responses and their stimuli (stimulus encoding). Beyond CRFs, this novel neural probe may enable new spatiotemporal 3D volumetric mapping to address, with cellular resolution, how the brain coordinates function.

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Section: Introductionmentioning

confidence: 99%

Epi-Intra neural probes with glassy carbon microelectrodes help elucidate neural coding and stimulus encoding in 3D volume of tissue

et al. 2020

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“…It is possible that repeated pulses act to engage larger reverberating or oscillating networks with increasing amplitude while the mechanisms underlying responses to SPES can reach a limit by not engaging these widespread networks. Further tests, including the use of microelectrode recordings to parse individual neuronal activity during these different stimulation approaches [92].…”

Section: Discussionmentioning

confidence: 99%

“…We posit there could be an effect of being closer to the axon hillocks of large pyramidal cells in cortical layers 4-6 and that the grey-white boundary is a convergence point for multiple output neurons or is a site with a higher concentration of excitatory versus inhibitory contributions which could explain the peak local responses [83]. To test these ideas, modelling in combination with cytoarchitectonic maps are likely necessary [84,85] in addition to sampling of neural data on microscale levels [14,92,95].…”

Section: Discussionmentioning

confidence: 99%

Impact of stimulation location relative to grey and white matter on single pulse electrical stimulation responses in the human brain

Paulk

Zelmann

Crocker

et al. 2021

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Background: Electrical neuromodulation is an increasingly common therapy for a wide variety of neuropsychiatric diseases. Unfortunately, therapeutic efficacy is inconsistent, possibly a result of our limited understanding of the mechanisms and the massive stimulation parameter space. Objective/Hypothesis: To better understand the role different parameters play in inducing a response, we systematically examined single pulse-induced cortico-cortico evoked potentials (CCEP) as a function of stimulation amplitude, duration and location in the brain and relative to grey and white matter. Methods: We measured voltage peak amplitudes and area under the curve of intracranially recorded stimulation responses as a function of distance from the stimulation site, pulse width, current injected, location relative to grey and white matter, and brain region stimulated (N=52, n=719 stimulation sites). Results: Increasing stimulation pulse width increased response values near the stimulation location. Increasing stimulation amplitude (current) increased responses nonlinearly. Locally (<15 mm from the stimulation site), stimulation closer to the grey matter-white matter boundary induced larger responses. In contrast, for distant sites (>15 mm), white matter stimulation consistently produced larger responses than stimulation in or near grey matter. These relationships were different between cingulate, lateral prefrontal, and lateral temporal cortical stimulation. Conclusion: These results demonstrate the importance of location and stimulation parameters in inducing a specific output and indicate that a stronger local response may require stimulation in the grey-white boundary while stimulation in the white matter may be needed for network activation, suggesting that stimulation location can be tailored for a specific outcome, key to informed neuromodulatory therapy.

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“…With the advent of genetically encoded calcium probes of neuronal activity (Dana et al 2019, Qian et al 2020), computational methods for extraction of spikes from calcium signals (Giovannucci et al 2019), microscopic tools for large-scale imaging (reviewed in (Abdelfattah et al 2022)) and electrode array technology (Hong & Lieber 2019, Lee et al, Vazquez-Guardado et al 2020), there has been a growing appreciation of the need to reconcile optical and electrophysiological measurements of neuronal spikes (Siegle et al 2021). Among the novel electrode technologies are minimally invasive devices that can be placed on the cortical surface to record extracellular electrical potentials, which can be then separated into high-frequency spiking activity and low-frequency “brain waves” (Buzsaki et al 2015, Choi et al 2019, Ganji et al 2019, Hermiz et al 2020, Hong & Lieber 2019, Jun et al 2017, Khodagholy et al 2015, Paulk et al 2021, Tchoe et al 2022). Because the top layer of cerebral cortex (layer 1, L1) has low density of neuronal cell bodies, spiking activity picked up from the cortical surface has been attributed to neurons with cell bodies located in layer 2/3 (L2/3; ~100 μm deep in the mouse) (Khodagholy et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Imaging through Windansee electrode arrays reveals a small fraction of local neurons following surface MUA

Thunemann

Hossain

Ness

et al. 2022

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Prior studies have shown that neuronal spikes can be recorded with microelectrode arrays placed on the cortical surface. However, the etiology of these spikes remains unclear. Because the top cortical layer (layer 1) contains very few neuronal cell bodies, it has been proposed that these spikes originate from neurons with cell bodies in layer 2. To address this question, we combined two-photon calcium imaging with electrophysiological recordings from the cortical surface in awake mice using chronically implanted PEDOT:PSS electrode arrays on transparent parylene C substrate. Our electrode arrays (termed Windansee) were integrated with cortical windows offering see-through optical access while also providing measurements of local field potentials (LFP) and multiunit activity (MUA) from the cortical surface. To enable longitudinal data acquisition, we have developed a mechanical solution for installation, connectorization, and protection of Windansee devices aiming for an unhindered access for high numerical aperture microscope objectives and a lifetime of several months while worn by a mouse. Contrary to the common notion, our measurements revealed that only a small fraction of layer 2 neurons from the sampled pool (~13%) faithfully followed MUA recorded from the surface above the imaging field-of-view. Surprised by this result, we turned to computational modeling for an alternative explanation of the MUA signal. Using realistic modeling of neurons with back-propagating dendritic properties, we computed the extracellular action potential at the cortical surface due to firing of local cortical neurons and compared the result to that due to axonal inputs to layer 1. Assuming the literature values for the cell/axon density and firing rates, our modeling results show that surface MUA due to axonal inputs is over an order of magnitude larger than that due to firing of layer 2 pyramidal neurons. Thus, a combination of surface MUA recordings with two-photon calcium imaging can provide complementary information about the input to a cortical column and the local circuit response. Cortical layer I plays an important role in integration of a broad range of cortico-cortical, thalamocortical and neuromodulatory inputs. Therefore, detecting their activity as MUA while combining electrode recording with two-photon imaging using optically transparent surface electrode arrays would facilitate studies of the input/output relationship in cortical circuits, inform computational circuit models, and improve the accuracy of the next generation brain-machine interfaces.

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Microscale physiological events on the human cortical surface

Cited by 5 publications

References 92 publications

Epi-Intra neural probes with glassy carbon microelectrodes help elucidate neural coding and stimulus encoding in 3D volume of tissue

Epi-Intra neural probes with glassy carbon microelectrodes help elucidate neural coding and stimulus encoding in 3D volume of tissue

Impact of stimulation location relative to grey and white matter on single pulse electrical stimulation responses in the human brain

Imaging through Windansee electrode arrays reveals a small fraction of local neurons following surface MUA

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