Lack of context modulation in human single neuron responses in the medial temporal lobe

Hernan G Rey; Theofanis I Panagiotaropoulos; Lorenzo Gutierrez; Fernando J Chaure; Alejandro Nasimbera; Santiago Cordisco; Fabian Nishida; Antonio Valentin; Gonzalo Alarcon; Mark P Richardson; Silvia Kochen; Rodrigo Quian Quiroga

doi:10.1016/j.celrep.2024.115218

Lack of context modulation in human single neuron responses in the medial temporal lobe

Cell Rep. 2025 Jan 15;44(1):115218. doi: 10.1016/j.celrep.2024.115218. Online ahead of print.

Affiliations

¹ Centre for Systems Neuroscience, University of Leicester, Leicester, UK; Departments of Neurosurgery, Biomedical Engineering, and Pharmacology and Toxicology, Medical College of Wisconsin, Milwaukee, WI 53226, USA.
² Centre for Systems Neuroscience, University of Leicester, Leicester, UK; Cognitive Neuroimaging Unit, INSERM, Universite Paris-Sud, Universite Paris-Saclay, Paris, France; Department of Psychology, National and Kapodistrian University of Athens, 15784 Athens, Greece; Centre for Basic Research, Biomedical Research Foundation of the Academy of Athens (BRFAA), Athens, Greece.
³ Centre for Systems Neuroscience, University of Leicester, Leicester, UK; Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁴ Centre for Systems Neuroscience, University of Leicester, Leicester, UK; Institute of Biomedical Engineering, University of Buenos Aires, Buenos Aires, Argentina.
⁵ ENyS, CEMET, Av. Calchaquí 5401, Buenos Aires 1888, Argentina.
⁶ ENyS, CEMET, Av. Calchaquí 5401, Buenos Aires 1888, Argentina; Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁷ Department of Basic and Clinical Neuroscience, Institute of Psychiatry Psychology and Neuroscience, King's College London, London, UK.
⁸ Department of Clinical Neurophysiology. Royal Manchester Children's Hospital, Manchester, UK.
⁹ ENyS, CEMET, Av. Calchaquí 5401, Buenos Aires 1888, Argentina; Epilepsy Centre, El Cruce Hospital, Buenos Aires, Argentina.
¹⁰ Centre for Systems Neuroscience, University of Leicester, Leicester, UK; Hospital Del Mar Medical Research Institute (IMIM), Barcelona, Spain; Institució Catalana de Recerca I Estudis Avançats (ICREA), Barcelona, Spain; Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China. Electronic address: [email protected].

PMID: 39823228
DOI: 10.1016/j.celrep.2024.115218

Abstract

In subjects implanted with intracranial electrodes, we use two different stories involving the same person (or place) to evaluate whether and to what extent context modulates human single-neuron responses. Nearly all neurons (97% during encoding and 100% during recall) initially responding to a person/place do not modulate their response with context. Likewise, nearly none (<1%) of the initially non-responsive neurons show conjunctive coding, responding to particular persons/places in a particular context during the tasks. In line with these findings, taking all neurons together it is possible to decode the person/place being depicted in each story, but not the particular story. Moreover, the neurons show consistent results across encoding and recall of the stories and during passive viewing of pictures. These results suggest a context invariant, non-conjunctive coding of memories at the single-neuron level in the human hippocampus and amygdala, in contrast to what has been described in other species.

Keywords: CP: Neuroscience; context modulation; episodic memory; hippocampus; human memory; human single-cell recordings; memory; neural coding; pattern separation.