Microscale Physiological Events on the Human Cortical Surface

Author:

Paulk Angelique C1ORCID,Yang Jimmy C12,Cleary Daniel R345,Soper Daniel J1,Halgren Mila16,O’Donnell Alexandra R1,Lee Sang Heon7,Ganji Mehran7,Ro Yun Goo7,Oh Hongseok7,Hossain Lorraine8,Lee Jihwan7,Tchoe Youngbin7,Rogers Nicholas4,Kiliç Kivilcim3,Ryu Sang Baek2,Lee Seung Woo2,Hermiz John7,Gilja Vikash7,Ulbert István910,Fabó Daniel11,Thesen Thomas1213,Doyle Werner K13,Devinsky Orrin13,Madsen Joseph R14,Schomer Donald L15,Eskandar Emad N216,Lee Jong Woo17,Maus Douglas1,Devor Anna3,Fried Shelley I218,Jones Pamela S2,Nahed Brian V2,Ben-Haim Sharona5,Bick Sarah K2,Richardson Robert Mark2ORCID,Raslan Ahmed M19,Siler Dominic A19,Cahill Daniel P2,Williams Ziv M2,Cosgrove G Rees20,Dayeh Shadi A5821,Cash Sydney S1

Affiliation:

1. Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USA

2. Department of Neurosurgery, Massachusetts General Hospital, Boston, MA 02114, USA

3. Departments of Neurosciences and Radiology, University of California San Diego, La Jolla, CA 92093, USA

4. Department of Physics, University of California San Diego, La Jolla, CA 92093, USA

5. Department of Neurosurgery, University of California San Diego, La Jolla, CA 92093, USA

6. McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA

7. Department of Electrical and Computer Engineering, University of California San Diego, La Jolla, CA 92093, USA

8. Materials Science and Engineering Program, University of California San Diego, La Jolla, CA 92093, USA

9. Research Centre for Natural Sciences, Institute of Cognitive Neuroscience and Psychology, 1519 Budapest, Hungary

10. Pázmány Péter Catholic University, Faculty of Information Technology and Bionics, H-1444 Budapest, Hungary

11. Epilepsy Centrum, National Institute of Clinical Neurosciences, 1145 Budapest, Hungary

12. Department of Biomedical Sciences, University of Houston College of Medicine, Houston, TX 77204, USA

13. Comprehensive Epilepsy Center, New York University School of Medicine, New York City, NY 10016, USA

14. Departments of Neurosurgery, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA

15. Department of Neurology, Beth Israel Deaconess Medical Center, Boston, MA 02215, USA

16. Albert Einstein College of Medicine, Montefiore Medical Center, Department of Neurosurgery, Bronx, NY 10467, USA

17. Department of Neurology, Brigham and Women's Hospital, Boston, MA 02115, USA

18. Boston VA Healthcare System, 150 South Huntington Avenue, Boston, MA 02130, USA

19. Department of Neurological Surgery, Oregon Health and Science University, Portland, OR 97239, USA

20. Department of Neurosurgery, Brigham and Women's Hospital, Boston, MA 02115, USA

21. Department of Nanoengineering, University of California San Diego, La Jolla, CA 92093, USA

Abstract

Abstract Despite ongoing advances in our understanding of local single-cellular and network-level activity of neuronal populations in the human brain, extraordinarily little is known about their “intermediate” microscale local circuit dynamics. Here, we utilized ultra-high-density microelectrode arrays and a rare opportunity to perform intracranial recordings across multiple cortical areas in human participants to discover three distinct classes of cortical activity that are not locked to ongoing natural brain rhythmic activity. The first included fast waveforms similar to extracellular single-unit activity. The other two types were discrete events with slower waveform dynamics and were found preferentially in upper cortical layers. These second and third types were also observed in rodents, nonhuman primates, and semi-chronic recordings from humans via laminar and Utah array microelectrodes. The rates of all three events were selectively modulated by auditory and electrical stimuli, pharmacological manipulation, and cold saline application and had small causal co-occurrences. These results suggest that the proper combination of high-resolution microelectrodes and analytic techniques can capture neuronal dynamics that lay between somatic action potentials and aggregate population activity. Understanding intermediate microscale dynamics in relation to single-cell and network dynamics may reveal important details about activity in the full cortical circuit.

Funder

U.S. Army Research Office and Defense Advanced Research Projects Agency

National Institutes of Health

ECOR

Tiny Blue Dot Foundation

NSF-CAREER

BRAIN Initiative

Hungarian Brain Research Program

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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