A corollary discharge mediates saccade-related inhibition of single units in mnemonic structures of the human brain

Chaim N Katz; Andrea G P Schjetnan; Kramay Patel; Victoria Barkley; Kari L Hoffman; Suneil K Kalia; Katherine D Duncan; Taufik A Valiante

doi:10.1016/j.cub.2022.06.015

A corollary discharge mediates saccade-related inhibition of single units in mnemonic structures of the human brain

Curr Biol. 2022 Jul 25;32(14):3082-3094.e4. doi: 10.1016/j.cub.2022.06.015. Epub 2022 Jul 1.

Authors

Chaim N Katz¹, Andrea G P Schjetnan², Kramay Patel³, Victoria Barkley², Kari L Hoffman⁴, Suneil K Kalia⁵, Katherine D Duncan⁶, Taufik A Valiante⁷

Affiliations

¹ Krembil Brain Institute, Toronto Western Hospital (TWH), Toronto, ON M5T 1M8, Canada; Institute of Biomedical Engineering, University of Toronto, Toronto, ON M5S 3G9, Canada; CRANIA, University Health Network and University of Toronto, Toronto, ON M5G 2A2, Canada; Faculty of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada.
² Krembil Brain Institute, Toronto Western Hospital (TWH), Toronto, ON M5T 1M8, Canada; CRANIA, University Health Network and University of Toronto, Toronto, ON M5G 2A2, Canada.
³ Krembil Brain Institute, Toronto Western Hospital (TWH), Toronto, ON M5T 1M8, Canada; Institute of Biomedical Engineering, University of Toronto, Toronto, ON M5S 3G9, Canada; Faculty of Medicine, University of Toronto, Toronto, ON M5S 1A8, Canada; CRANIA, University Health Network and University of Toronto, Toronto, ON M5G 2A2, Canada.
⁴ Department of Psychology, Vanderbilt University, Nashville, TN 37240, USA.
⁵ Krembil Brain Institute, Toronto Western Hospital (TWH), Toronto, ON M5T 1M8, Canada; Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, ON M5S 1A1, Canada; CRANIA, University Health Network and University of Toronto, Toronto, ON M5G 2A2, Canada; The KITE Research Institute, University Health Network, Toronto, ON M5G 2A2, Canada.
⁶ Department of Psychology, University of Toronto, Toronto, ON M5S 3G3, Canada.
⁷ Krembil Brain Institute, Toronto Western Hospital (TWH), Toronto, ON M5T 1M8, Canada; Institute of Biomedical Engineering, University of Toronto, Toronto, ON M5S 3G9, Canada; Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, ON M5S 1A1, Canada; Institute of Medical Sciences, University of Toronto, Toronto, ON M5S 1A8, Canada; Electrical and Computer Engineering, University of Toronto, Toronto, ON M5S 3G4, Canada; CRANIA, University Health Network and University of Toronto, Toronto, ON M5G 2A2, Canada; The KITE Research Institute, University Health Network, Toronto, ON M5G 2A2, Canada; Max Planck-University of Toronto Center for Neural Science and Technology, Toronto, ON, Canada. Electronic address: taufik.valiante@uhn.ca.

PMID: 35779529
DOI: 10.1016/j.cub.2022.06.015

Abstract

Despite the critical link between visual exploration and memory, little is known about how neuronal activity in the human mesial temporal lobe (MTL) is modulated by saccades. Here, we characterize saccade-associated neuronal modulations, unit-by-unit, and contrast them to image onset and to occipital lobe neurons. We reveal evidence for a corollary discharge (CD)-like modulatory signal that accompanies saccades, inhibiting/exciting a unique population of broad-/narrow-spiking units, respectively, before and during saccades and with directional selectivity. These findings comport well with the timing, directional nature, and inhibitory circuit implementation of a CD. Additionally, by linking neuronal activity to event-related potentials (ERPs), which are directionally modulated following saccades, we recontextualize the ERP associated with saccades as a proxy for both the strength of inhibition and saccade direction, providing a mechanistic underpinning for the more commonly recorded saccade-related ERP in the human brain.

Keywords: corollary discharge; epilepsy; hippocampus; human; inhibition; microwire; nucleus reuniens; sEEG; saccade; single unit.

MeSH terms

Brain*
Humans
Inhibition, Psychological
Neurons / physiology
Photic Stimulation
Reaction Time / physiology
Saccades*