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• W4367693757 abstract "•Microelectrode arrays are implanted in patients undergoing awake brain surgery•Open craniotomies grant access to large parts of the left-hemispheric cortex•High-quality neuronal activity is obtained at multiple levels of resolution•Human parietal cortex neurons are tuned to non-symbolic and symbolic numbers There are vast gaps in our understanding of the organization and operation of the human nervous system at the level of individual neurons and their networks. Here, we report reliable and robust acute multichannel recordings using planar microelectrode arrays (MEAs) implanted intracortically in awake brain surgery with open craniotomies that grant access to large parts of the cortical hemisphere. We obtained high-quality extracellular neuronal activity at the microcircuit, local field potential level and at the cellular, single-unit level. Recording from the parietal association cortex, a region rarely explored in human single-unit studies, we demonstrate applications on these complementary spatial scales and describe traveling waves of oscillatory activity as well as single-neuron and neuronal population responses during numerical cognition, including operations with uniquely human number symbols. Intraoperative MEA recordings are practicable and can be scaled up to explore cellular and microcircuit mechanisms of a wide range of human brain functions. There are vast gaps in our understanding of the organization and operation of the human nervous system at the level of individual neurons and their networks. Here, we report reliable and robust acute multichannel recordings using planar microelectrode arrays (MEAs) implanted intracortically in awake brain surgery with open craniotomies that grant access to large parts of the cortical hemisphere. We obtained high-quality extracellular neuronal activity at the microcircuit, local field potential level and at the cellular, single-unit level. Recording from the parietal association cortex, a region rarely explored in human single-unit studies, we demonstrate applications on these complementary spatial scales and describe traveling waves of oscillatory activity as well as single-neuron and neuronal population responses during numerical cognition, including operations with uniquely human number symbols. Intraoperative MEA recordings are practicable and can be scaled up to explore cellular and microcircuit mechanisms of a wide range of human brain functions. There are vast gaps in our understanding of the organization and operation of the human nervous system at the level of individual neurons and their networks. Limited opportunities to directly access the human brain call for multidisciplinary collaborations that combine expertise in neuroscience and clinical medicine to invasively measure neuronal activity with single-unit resolution.1Cash S.S. Hochberg L.R. The emergence of single neurons in clinical neurology.Neuron. 2015; 86: 79-91https://doi.org/10.1016/j.neuron.2015.03.058Abstract Full Text Full Text PDF PubMed Scopus (51) Google Scholar This approach has been most fruitful in patients with medically intractable epilepsy implanted with microwire bundles2Fu Z. Beam D. Chung J.M. Reed C.M. Mamelak A.N. Adolphs R. Rutishauser U. The geometry of domain-general performance monitoring in the human medial frontal cortex.Science. 2022; 376: eabm9922https://doi.org/10.1126/science.abm9922Crossref PubMed Scopus (13) Google Scholar,3Minxha J. Adolphs R. Fusi S. Mamelak A.N. Rutishauser U. Flexible recruitment of memory-based choice representations by the human medial frontal cortex.Science. 2020; 368: eaba3313https://doi.org/10.1126/science.aba3313Crossref PubMed Scopus (36) Google Scholar,4Kamiński J. Sullivan S. Chung J.M. Ross I.B. Mamelak A.N. Rutishauser U. Persistently active neurons in human medial frontal and medial temporal lobe support working memory.Nat. Neurosci. 2017; 20: 590-601https://doi.org/10.1038/nn.4509Crossref PubMed Scopus (114) Google Scholar,5Rutishauser U. Ross I.B. Mamelak A.N. Schuman E.M. Human memory strength is predicted by theta-frequency phase-locking of single neurons.Nature. 2010; 464: 903-907https://doi.org/10.1038/nature08860Crossref PubMed Scopus (434) Google Scholar,6Kutter E.F. Bostroem J. Elger C.E. Mormann F. Nieder A. Single neurons in the human brain encode numbers.Neuron. 2018; 100: 753-761.e4https://doi.org/10.1016/j.neuron.2018.08.036Abstract Full Text Full Text PDF PubMed Scopus (60) Google Scholar,7Kornblith S. Quian Quiroga R. Koch C. Fried I. Mormann F. Persistent single-neuron activity during working memory in the human medial temporal lobe.Curr. Biol. 2017; 27: 1026-1032https://doi.org/10.1016/j.cub.2017.02.013Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar,8Sheth S.A. Mian M.K. Patel S.R. Asaad W.F. Williams Z.M. Dougherty D.D. Bush G. Eskandar E.N. Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation.Nature. 2012; 488: 218-221https://doi.org/10.1038/nature11239Crossref PubMed Scopus (303) Google Scholar and in patients with movement disorders undergoing deep brain stimulation (DBS).9Jamali M. Grannan B.L. Fedorenko E. Saxe R. Báez-Mendoza R. Williams Z.M. Single-neuronal predictions of others' beliefs in humans.Nature. 2021; 591: 610-614https://doi.org/10.1038/s41586-021-03184-0Crossref PubMed Scopus (37) Google Scholar,10Jamali M. Grannan B. Haroush K. Moses Z.B. Eskandar E.N. Herrington T. Patel S. Williams Z.M. Dorsolateral prefrontal neurons mediate subjective decisions and their variation in humans.Nat. Neurosci. 2019; 22: 1010-1020https://doi.org/10.1038/s41593-019-0378-3Crossref PubMed Scopus (14) Google Scholar,11Zaghloul K.A. Blanco J.A. Weidemann C.T. McGill K. Jaggi J.L. Baltuch G.H. Kahana M.J. Human substantia nigra neurons encode unexpected financial rewards.Science. 2009; 323: 1496-1499https://doi.org/10.1126/science.1167342Crossref PubMed Scopus (165) Google Scholar Two crucial challenges persist, however, in the investigation of the cellular and circuit physiology of human brain functions. First, epilepsy and DBS surgeries do not provide comprehensive brain coverage, leading to strong focusing of current human single-unit studies on the medial temporal lobe (MTL) and on small circumscribed regions of the frontal lobe. Second, reliable and robust recording technology is still lacking, meaning that clinicians must be trained on increasingly complex devices that necessitate significant modifications to standardized and proven surgical procedures.12Paulk A.C. Kfir Y. Khanna A.R. Mustroph M.L. Trautmann E.M. Soper D.J. Stavisky S.D. Welkenhuysen M. Dutta B. Shenoy K.V. et al.Large-scale neural recordings with single neuron resolution using Neuropixels probes in human cortex.Nat. Neurosci. 2022; 25: 252-263https://doi.org/10.1038/s41593-021-00997-0Crossref PubMed Scopus (37) Google Scholar,13Chung J.E. Sellers K.K. Leonard M.K. Gwilliams L. Xu D. Dougherty M.E. Kharazia V. Metzger S.L. Welkenhuysen M. Dutta B. Chang E.F. High-density single-unit human cortical recordings using the Neuropixels probe.Neuron. 2022; 110: 2409-2421.e3https://doi.org/10.1016/j.neuron.2022.05.007Abstract Full Text Full Text PDF PubMed Scopus (6) Google Scholar Broad access to the human cortex in large patient groups combined with easy-to-implement methods would greatly accelerate progress in researching the neuronal basis of human brain functions. Here, we demonstrate acute recordings from planar multichannel microelectrode arrays (Utah MEAs) implanted intracortically in patients awake for removal of left-hemispheric brain tumors. Tumor surgeries with open craniotomies expose large areas of the cortex and allow flexible placement of recording devices, meaning that electrode positions can be adapted to research questions, not vice versa. Awake surgeries with intraoperative functional mapping minimize the risk of postoperative deficits by delineating functionally important regions and thus increase the precision of tumor resection.14Sanai N. Mirzadeh Z. Berger M.S. Functional outcome after language mapping for glioma resection.N. Engl. J. Med. 2008; 358: 18-27https://doi.org/10.1056/NEJMoa067819Crossref PubMed Scopus (815) Google Scholar Patients undergoing awake surgery can perform a wide variety of tasks tapping into sensorimotor functions, visuospatial functions, language, and other higher cognitive functions.15Mandonnet E. Herbet G. Intraoperative Mapping of Cognitive Networks. Springer, 2021Crossref Google Scholar Penetrating, intracortical MEAs are widely used for chronic measurements of single-unit and population activity in non-human primates16Chen X. Wang F. Fernandez E. Roelfsema P.R. Shape perception via a high-channel-count neuroprosthesis in monkey visual cortex.Science. 2020; 370: 1191-1196https://doi.org/10.1126/science.abd7435Crossref PubMed Scopus (86) Google Scholar,17Mitz A.R. Bartolo R. Saunders R.C. Browning P.G. Talbot T. Averbeck B.B. High channel count single-unit recordings from nonhuman primate frontal cortex.J. Neurosci. Methods. 2017; 289: 39-47https://doi.org/10.1016/j.jneumeth.2017.07.001Crossref PubMed Scopus (25) Google Scholar and have shown potential for clinical applications18Schevon C.A. Tobochnik S. Eissa T. Merricks E. Gill B. Parrish R.R. Bateman L.M. McKhann Jr., G.M. Emerson R.G. Trevelyan A.J. Multiscale recordings reveal the dynamic spatial structure of human seizures.Neurobiol. Dis. 2019; 127: 303-311https://doi.org/10.1016/j.nbd.2019.03.015Crossref PubMed Scopus (31) Google Scholar,19Truccolo W. Donoghue J.A. Hochberg L.R. Eskandar E.N. Madsen J.R. Anderson W.S. Brown E.N. Halgren E. Cash S.S. Single-neuron dynamics in human focal epilepsy.Nat. Neurosci. 2011; 14: 635-641https://doi.org/10.1038/nn.2782Crossref PubMed Scopus (364) Google Scholar as well as for neurorestorative brain-computer interfaces (BCIs) in humans.20Willett F.R. Avansino D.T. Hochberg L.R. Henderson J.M. Shenoy K.V. High-performance brain-to-text communication via handwriting.Nature. 2021; 593: 249-254https://doi.org/10.1038/s41586-021-03506-2Crossref PubMed Scopus (188) Google Scholar,21Pandarinath C. Nuyujukian P. Blabe C.H. Sorice B.L. Saab J. Willett F.R. Hochberg L.R. Shenoy K.V. Henderson J.M. High performance communication by people with paralysis using an intracortical brain-computer interface.Elife. 2017; 6: e18554https://doi.org/10.7554/eLife.18554Crossref PubMed Scopus (247) Google Scholar,22Hochberg L.R. Serruya M.D. Friehs G.M. Mukand J.A. Saleh M. Caplan A.H. Branner A. Chen D. Penn R.D. Donoghue J.P. Neuronal ensemble control of prosthetic devices by a human with tetraplegia.Nature. 2006; 442: 164-171https://doi.org/10.1038/nature04970Crossref PubMed Scopus (2464) Google Scholar,23Aflalo T. Kellis S. Klaes C. Lee B. Shi Y. Pejsa K. Shanfield K. Hayes-Jackson S. Aisen M. Heck C. et al.Decoding motor imagery from the posterior parietal cortex of a tetraplegic human.Science. 2015; 348: 906-910https://doi.org/10.1126/science.aaa5417Crossref PubMed Scopus (359) Google Scholar,24Fernández E. Alfaro A. Soto-Sánchez C. Gonzalez-Lopez P. Lozano A.M. Peña S. Grima M.D. Rodil A. Gómez B. Chen X. et al.Visual percepts evoked with an intracortical 96-channel microelectrode array inserted in human occipital cortex.J. Clin. Invest. 2021; 131: e151331https://doi.org/10.1172/JCI151331Crossref PubMed Scopus (37) Google Scholar,25Flesher S.N. Collinger J.L. Foldes S.T. Weiss J.M. Downey J.E. Tyler-Kabara E.C. Bensmaia S.J. Schwartz A.B. Boninger M.L. Gaunt R.A. Intracortical microstimulation of human somatosensory cortex.Sci. Transl. Med. 2016; 8: 361ra141https://doi.org/10.1126/scitranslmed.aaf8083Crossref PubMed Scopus (374) Google Scholar Despite these successes, acute intraoperative MEA recordings to investigate human brain functions have not been reported. Cortical microtrauma and neuronal “stunning” are believed to prohibit measurements with these devices shortly after implantation.26Fernández E. Greger B. House P.A. Aranda I. Botella C. Albisua J. Soto-Sánchez C. Alfaro A. Normann R.A. Acute human brain responses to intracortical microelectrode arrays: challenges and future prospects.Front. Neuroeng. 2014; 7: 24https://doi.org/10.3389/fneng.2014.00024Crossref PubMed Scopus (88) Google Scholar,27House P.A. MacDonald J.D. Tresco P.A. Normann R.A. Acute microelectrode array implantation into human neocortex: preliminary technique and histological considerations.Neurosurg. Focus. 2006; 20: E4https://doi.org/10.3171/foc.2006.20.5.5Crossref PubMed Scopus (58) Google Scholar In this study, we show that these obstacles can be overcome with appropriate choice of the arrays’ geometrical configuration. We hypothesized that the degree of tissue impact, and thus the quality of acquired neuronal signals, would depend on the number of implanted electrodes and in particular the electrode density; increased electrode spacing (lower density) might result in larger pressure at the individual electrode tip during implantation (given the same force applied to the back of the array) and thus allow faster and less traumatic cortical penetration. We therefore systematically compared higher-density MEAs (standard array, 96 electrodes with 400-μm spacing) and lower-density MEAs (custom array, 25 electrodes with 800-μm spacing). We found that all implanted arrays recorded high-quality extracellular signals at the microcircuit level (local field potentials [LFPs]). MEAs with increased electrode spacing, however, outperformed standard arrays with higher densities and also captured activity at the cellular, single-unit level. To demonstrate applications on these complementary spatial scales, we describe oscillatory dynamics in the form of waves of activity traveling across the human parietal association cortex, a region rarely explored in human single-unit studies, and investigate single-neuron mechanisms of numerical cognition, including operations with uniquely human symbolic quantities. Our findings demonstrate that intraoperative MEA recording technology is suited to provide the high-volume recordings necessary to advance translational research on the cellular and microcircuit basis of a wide range of human brain functions. Awake surgeries with open craniotomies enable direct, controlled investigations of human brain functions while the patients are alert and can perform tasks of varying complexity15Mandonnet E. Herbet G. Intraoperative Mapping of Cognitive Networks. Springer, 2021Crossref Google Scholar (Figure 1A). Craniotomies overlap in particular over the motor cortical regions and over the posterior frontal lobes (Figure 1B). They can extend anteriorly to the frontal pole and posteriorly to the parieto-occipital junction, dorsally to the inter-hemispheric fissure (midline), and ventrally to the temporal lobe. Typical craniotomies expose large regions of cortex (several tens of square centimeters), yielding broad access to the human brain. Infrared thermal imaging during a representative surgery verified that physiological temperatures are maintained at the cortical surface (Figure 1C). We performed a total of 13 acute MEA implantations in patients undergoing surgery for brain tumor resection (one array per patient), eight of whom were operated on while awake (Table S1). Except for the procedures related to array implantation, the course of the surgery was not changed. Following skin incision, preparation, and opening of the skull and dura mater, but before awakening the patient from anesthesia, we placed the array’s pedestal next to the craniotomy, anchored it with skull screws, and positioned the MEA over the target cortical area (Figure 1D). Reference wires were inserted under the dura. We intended for the implantation site to lie as remotely as possible from the bulk tumor tissue but still within the pre-operatively determined resection area. The array was then pneumatically inserted and covered with saline-irrigated strips (Figure 1E) until explantation, typically when tumor resection started. With established and practiced procedures, the implantation could be performed in less than 10 min. We encountered no adverse clinical events in connection to MEA implantation or recordings, neither during the surgery nor during routine patient follow-up over several months to years. For each participant, the implantation site was reconstructed using intraoperative photographic documentation as well as pre-operative structural MRI. Three implantations were located in the frontal cortex and 10 in the parietal cortex (Table S1). Examples of implantations in the middle frontal gyrus, the supramarginal gyrus, and the angular gyrus are shown in Figure 1F. We histologically analyzed three implantations (Table S1). Grids of electrode tracts could be clearly identified from the penetration of the pia mater along the course of the shafts to, in some instances, the tip of the electrode (Figure 1G). The majority of the electrode tracts reached deeper cortical layers. In two patients, cortical tissue surrounding the electrodes showed no structural abnormalities across the entire array. In one patient, we observed small microbleeding without a space-occupying effect along several electrode tracts as well as in deep cortical layers26Fernández E. Greger B. House P.A. Aranda I. Botella C. Albisua J. Soto-Sánchez C. Alfaro A. Normann R.A. Acute human brain responses to intracortical microelectrode arrays: challenges and future prospects.Front. Neuroeng. 2014; 7: 24https://doi.org/10.3389/fneng.2014.00024Crossref PubMed Scopus (88) Google Scholar,27House P.A. MacDonald J.D. Tresco P.A. Normann R.A. Acute microelectrode array implantation into human neocortex: preliminary technique and histological considerations.Neurosurg. Focus. 2006; 20: E4https://doi.org/10.3171/foc.2006.20.5.5Crossref PubMed Scopus (58) Google Scholar (Figure 1H). However, these changes were strictly confined to the vicinity of the electrodes. We did not detect any pathology distant from the implantation site. In sum, implantation of intracortical MEAs in patients undergoing awake brain surgery is safe and practicable, achieving broad and direct access to the neuronal networks of the human cortical left hemisphere. In the group of patients operated on for awake tumor resection, we discontinued anesthesia following MEA implantation. We began recording wide-band extracellular activity (Figure 2A) as soon as the patients were alert and able to engage in conversation with the clinical team and prior to cortical electrostimulation for mapping of language-associated areas. Typically, the arrays had been settling for 30–40 min. We emphasize that the surgery was not prolonged by this time period; we merely used the awakening time to allow for the signals to develop and stabilize. We first sought to evaluate the ability to detect the activity of individual neurons (i.e., spikes), present in the high-frequency signal components (high-pass filter, 250 Hz; Figures 2B–2F). We compared two different MEA configurations: a standard, higher-density array with 400-μm electrode spacing (pitch) and 96 active channels on a 10 × 10 grid and a custom, lower-density array with 800 μm pitch and 25 channels (Figure 2C, left and right, respectively). Electrode lengths were 1.5 mm for both array types. We performed four implantations with each array type (Table S1). Technical difficulties with grounding (patient 08 [P08], higher-density array) and a medical complication not related to the implantation (P12, lower-density array) did not allow us to advance to neuronal recording in two surgeries. In one case, we observed an abrupt drop in signal quality a few minutes into data acquisition (P13, lower-density array), prompting us to omit this dataset from in-depth analysis. Qualitatively, prior to the unexplained event, the recording was not different from the other lower-density recordings. The likelihood of recording spiking activity varied significantly between array configurations. In an example higher-density array, spiking activity of sufficiently high amplitudes for subsequent waveform sorting was present in only a few channels (Figure 2D, left). In contrast, in an example lower-density array, spikes were detected on all electrodes (Figure 2D, right). Signal-to-noise ratios (SNRs) in this array were stable across the entire recording (25 min), with the exception of a single large electrical artifact leading to an increase in noise (Figures 2E, S1A, and S1B). This did not impact spike amplitudes, however, which remained stable during data acquisition. Across all successful recordings, this pattern was reproduced (Figure 2F); in three consecutive implantations with the higher-density array (five implantations including two anesthetized participants; Table S1), we did not observe appreciable spiking activity (2% of channels). In three consecutive implantations with the lower-density array (one recording not shown because of early termination; see above), we obtained spikes on the majority of channels (78% of channels; p < 0.001, Fisher’s exact test, higher-density vs. lower-density arrays). In the event that spiking activity could be recorded, SNRs were comparable (mean, 17.1 ± 0.9 dB and 16.8 ± 0.8 dB for higher-density and lower-density arrays, respectively; p = 0.91, two-tailed Wilcoxon test). Next, we evaluated the quality of LFPs, a measure of local network activity; i.e., the low-frequency component of our extracellular recordings (low-pass filter, 250 Hz; Figures 2G–2J). Epochs of increased LFP activity were readily detected in higher-density and lower-density arrays and across all channels (Figure 2H; same example arrays as in Figure 2D). In both array configurations, SNRs were high and displayed spatial clusters of similar signal strength. In the lower-density array, the clusters of high-spiking SNRs and high-LFP SNRs overlapped. As for the spiking activity, LFP signals were stable across the recording session and affected only momentarily because of a single electrical artifact (Figures 2I, S1A, and S1B). Across all successful recordings, LFP SNRs were very uniform across channels (mean 21.5 ± 0.1 dB and 21.7 ± 0.03 dB for higher-density and lower-density arrays, respectively; Figure 2J). Overall, electrical artifacts could be well controlled during intraoperative data acquisition. Very rarely, we observed a single high-amplitude “pop” across all electrodes that disrupted recordings for a few hundred milliseconds until the signals settled again (Figures S1A and S1B). Such electrode “pops” have been reported with sudden changes in impedance, likely related to the recording system electrostatically discharging when in contact with a liquid such as blood.28Colachis 4th, S.C. Dunlap C.F. Annetta N.V. Tamrakar S.M. Bockbrader M.A. Friedenberg D.A. Long-term intracortical microelectrode array performance in a human: a 5 year retrospective analysis.J. Neural. Eng. 2021; 18: 0460d7https://doi.org/10.1088/1741-2552/ac1addCrossref Scopus (15) Google Scholar 50-Hz line noise and its harmonics were regularly present in the recordings (Figures S1C and S1D) but could be efficiently removed by offline filtering. Good grounding (i.e., strong connection of the pedestal to the skull) significantly reduced the hum. Bad choice of grounding, in contrast, lead to signal contamination; e.g., by facial muscle activity (Figures S1E and S1F). To determine whether single units could be isolated from the population (multiunit) spiking activity (Figure 3A), we sorted the thresholded waveforms. Distinct waveform clusters representing well-isolated single units were separated from noise (Figures 3B and 3C) with little to no loss of spikes around the detection threshold (false negatives; Figure 3D; less than 5% of spikes in 74% of units), no contamination by spikes violating the refractory period (false positives; Figure 3E; less than 1% of spikes in all units), stable firing rates throughout the recording session (Figure 3F), and little to no mixing of spikes between different clusters (Figure 3G). Following this procedure, single units could be isolated on the majority of electrodes in the example lower-density array (Figure 3H), with two or more single units present on multiple channels. Across all analyzed recordings, single units were rarely picked up by the higher-density arrays (2% of channels) but frequently isolated on the lower-density arrays (62% of channels; p < 0.001, Fisher’s exact test, higher-density vs. lower-density arrays). On lower-density array electrodes with sortable spikes, we recorded, on average, 1.6 single units per electrode. While single neurons represent the brain’s elementary processing units, it is increasingly recognized that temporal coordination and synchronization of neuronal activity across distances is crucial, in particular for higher cognitive functions.29Fries P. Rhythms for cognition: communication through coherence.Neuron. 2015; 88: 220-235https://doi.org/10.1016/j.neuron.2015.09.034Abstract Full Text Full Text PDF PubMed Scopus (1279) Google Scholar Given their planar, grid-like configuration with well-defined spatial relationships between individual electrodes, MEAs are ideally suited to investigate the lateral propagation of activity in cortical networks. Several studies with chronic MEA recordings have reported waves of oscillatory brain activity that travel across the non-human primate and human cortex30Bhattacharya S. Brincat S.L. Lundqvist M. Miller E.K. Traveling waves in the prefrontal cortex during working memory.PLoS Comput. Biol. 2022; 18: e1009827https://doi.org/10.1371/journal.pcbi.1009827Crossref PubMed Scopus (12) Google Scholar,31Sato T.K. Nauhaus I. Carandini M. Traveling waves in visual cortex.Neuron. 2012; 75: 218-229https://doi.org/10.1016/j.neuron.2012.06.029Abstract Full Text Full Text PDF PubMed Scopus (152) Google Scholar,32Takahashi K. Saleh M. Penn R.D. Hatsopoulos N.G. Propagating waves in human motor cortex.Front. Hum. Neurosci. 2011; 5: 40https://doi.org/10.3389/fnhum.2011.00040Crossref PubMed Scopus (71) Google Scholar,33Rubino D. Robbins K.A. Hatsopoulos N.G. Propagating waves mediate information transfer in the motor cortex.Nat. Neurosci. 2006; 9: 1549-1557https://doi.org/10.1038/nn1802Crossref PubMed Scopus (318) Google Scholar and could reflect higher-order organization of neuronal processing in space and time.34Muller L. Chavane F. Reynolds J. Sejnowski T.J. Cortical travelling waves: mechanisms and computational principles.Nat. Rev. Neurosci. 2018; 19: 255-268https://doi.org/10.1038/nrn.2018.20Crossref PubMed Scopus (220) Google Scholar Examination of oscillatory beta activity (20 ± 1.5 Hz) in a higher-density recording showed LFP peaks temporally shifted across neighboring electrodes with ordered progression of activity from one side of the array to the other (top to bottom in Figure 4A). At each time point, LFP phases across the array could be approximated by a linear plane with non-zero slope aligned to the direction of activity propagation, in agreement with the notion of a traveling wave. We extracted and characterized such traveling waves in 500-ms epochs following presentation of visual stimuli (sample numbers; Figure 5) for theta (6–9 Hz) and beta LFP bands (15–35 Hz) LFP bands (Figures 4B–4E). Waves traveled in preferred directions (p < 0.001 in theta and beta, Hodges-Ajne test for nonuniformity) that were frequency band specific (Figure 4B). A second modal direction almost opposing the dominant primary direction suggested a spatial propagation axis (Figure 4B), in line with intracranial electroencephalogram (EEG) and electrocorticogram (ECoG) recordings35Das A. Myers J. Mathura R. Shofty B. Metzger B.A. Bijanki K. Wu C. Jacobs J. Sheth S.A. Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves.Elife. 2022; 11: e76702https://doi.org/10.7554/eLife.76702Crossref PubMed Scopus (8) Google Scholar,36Zhang H. Watrous A.J. Patel A. Jacobs J. Theta and alpha oscillations are traveling waves in the human neocortex.Neuron. 2018; 98: 1269-1281.e4https://doi.org/10.1016/j.neuron.2018.05.019Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar,37Zhang H. Jacobs J. Traveling theta waves in the human Hippocampus.J. Neurosci. 2015; 35: 12477-12487https://doi.org/10.1523/JNEUROSCI.5102-14.2015Crossref PubMed Scopus (88) Google Scholar and during ictal discharges in patients with epileptic seizures.38Liou J.Y. Smith E.H. Bateman L.M. McKhann G.M. Goodman R.R. Greger B. Davis T.S. Kellis S.S. House P.A. Schevon C.A. Multivariate regression methods for estimating velocity of ictal discharges from human microelectrode recordings.J. Neural. Eng. 2017; 14: 044001https://doi.org/10.1088/1741-2552/aa68a6Crossref PubMed Scopus (15) Google Scholar,39Smith E.H. Liou J.Y. Davis T.S. Merricks E.M. Kellis S.S. Weiss S.A. Greger B. House P.A. McKhann 2nd, G.M. Goodman R.R. et al.The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures.Nat. Commun. 2016; 7: 11098https://doi.org/10.1038/ncomms11098Crossref PubMed Scopus (78) Google Scholar With increasing oscillatory frequency, traveling waves were detected less often (Figure 4C) and showed higher propagation velocities (theta mean, 0.57 m/s; beta mean, 2.40 m/s; Figure 4D), again matching data from chronic MEA recordings (e.g., in the non-human primate prefrontal cortex30Bhattacharya S. Brincat S.L. Lundqvist M. Miller E.K. Traveling waves in the prefrontal cortex during working memory.PLoS Comput. Biol. 2022; 18: e1009827https://doi.org/10.1371/journal.pcbi.1009827Crossref PubMed Scopus (12) Google Scholar). Spatial phase gradients fit the plane model well in both frequency bands (measured by phase-gradient directionality [PGD]; theta mean, 0.72; beta mean, 0.62; Figure 4E). For comparison, we conducted the same analysis in a lower-density re" @default.
• W4367693757 created "2023-05-03" @default.
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• W4367693757 title "Human acute microelectrode array recordings with broad cortical access, single-unit resolution, and parallel behavioral monitoring" @default.
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