Distinctive biophysical features of human cell-types: insights from studies of neurosurgically resected brain tissue

Homeira Moradi Chameh; Madeleine Falby; Mandana Movahed; Keon Arbabi; Scott Rich; Liang Zhang; Jérémie Lefebvre; Shreejoy J Tripathy; Maurizio De Pittà; Taufik A Valiante

doi:10.3389/fnsyn.2023.1250834

Distinctive biophysical features of human cell-types: insights from studies of neurosurgically resected brain tissue

Front Synaptic Neurosci. 2023 Oct 4:15:1250834. doi: 10.3389/fnsyn.2023.1250834. eCollection 2023.

Authors

Homeira Moradi Chameh¹, Madeleine Falby^{1

2}, Mandana Movahed¹, Keon Arbabi^{2

3}, Scott Rich⁴, Liang Zhang¹, Jérémie Lefebvre^{1

5

6}, Shreejoy J Tripathy^{2

3

7}, Maurizio De Pittà^{1

8

9

10}, Taufik A Valiante^{1

2

11

12

13

14

15}

Affiliations

¹ Division of Clinical and Computational Neuroscience, Krembil Brain Institute, University Health Network (UHN), Toronto, ON, Canada.
² Institute of Medical Science, University of Toronto, Toronto, ON, Canada.
³ Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada.
⁴ Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, ON, Canada.
⁵ Department of Biology, University of Ottawa, Ottawa, ON, Canada.
⁶ Department of Mathematics, University of Toronto, Toronto, ON, Canada.
⁷ Department of Psychiatry, University of Toronto, Toronto, ON, Canada.
⁸ Department of Physiology, Temerty Faculty of Medicine, University of Toronto, Toronto, ON, Canada.
⁹ Basque Center for Applied Mathematics, Bilbao, Spain.
¹⁰ Faculty of Medicine, University of the Basque Country, Leioa, Spain.
¹¹ Institute of Biomedical Engineering, University of Toronto, Toronto, ON, Canada.
¹² Department of Electrical and Computer Engineering, University of Toronto, Toronto, ON, Canada.
¹³ Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, ON, Canada.
¹⁴ Center for Advancing Neurotechnological Innovation to Application (CRANIA), Toronto, ON, Canada.
¹⁵ Max Planck-University of Toronto Center for Neural Science and Technology, University of Toronto, Toronto, ON, Canada.

Abstract

Electrophysiological characterization of live human tissue from epilepsy patients has been performed for many decades. Although initially these studies sought to understand the biophysical and synaptic changes associated with human epilepsy, recently, it has become the mainstay for exploring the distinctive biophysical and synaptic features of human cell-types. Both epochs of these human cellular electrophysiological explorations have faced criticism. Early studies revealed that cortical pyramidal neurons obtained from individuals with epilepsy appeared to function "normally" in comparison to neurons from non-epilepsy controls or neurons from other species and thus there was little to gain from the study of human neurons from epilepsy patients. On the other hand, contemporary studies are often questioned for the "normalcy" of the recorded neurons since they are derived from epilepsy patients. In this review, we discuss our current understanding of the distinct biophysical features of human cortical neurons and glia obtained from tissue removed from patients with epilepsy and tumors. We then explore the concept of within cell-type diversity and its loss (i.e., "neural homogenization"). We introduce neural homogenization to help reconcile the epileptogenicity of seemingly "normal" human cortical cells and circuits. We propose that there should be continued efforts to study cortical tissue from epilepsy patients in the quest to understand what makes human cell-types "human".

Keywords: astrocyte; electrophysiology; epilepsy; human cortical tissue; morphology; pyramidal neurons; rodent cortical tissue; transcriptomic.

Publication types

Review

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Toronto General and Western Hospital Foundation, National Sciences and Engineering Research Council of Canada (NSERC Grants RGPIN-2020-07143 to TV) and generous support from the Centre for Addiction and Mental Health Discovery Fund.