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

• Published in: Cell reports (Cambridge) Vol. 44; no. 1; p. 115218
• Main Authors: Rey, Hernan G., Panagiotaropoulos, Theofanis I., Gutierrez, Lorenzo, Chaure, Fernando J., Nasimbera, Alejandro, Cordisco, Santiago, Nishida, Fabian, Valentin, Antonio, Alarcon, Gonzalo, Richardson, Mark P., Kochen, Silvia, Quian Quiroga, Rodrigo
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 28.01.2025; Cell Press
• Subjects: Adult; Amygdala - physiology; context modulation; Electrodes, Implanted; episodic memory; Female; hippocampus; Hippocampus - physiology; human memory; human single-cell recordings; Humans; Male; memory; Memory - physiology; Mental Recall - physiology; neural coding; Neurons - physiology; pattern separation; Temporal Lobe - cytology; Temporal Lobe - physiology; episodic memory; memory; hippocampus; CP: Neuroscience; neural coding; human single-cell recordings; context modulation; pattern separation; human memory
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2024.115218

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. [Display omitted] •In a naturalistic memory task, we show that hippocampal neurons are not modulated by context•We observe similar single-neuron responses to the same concepts in different tasks•Neurons do not show conjunctive coding (i.e., responding only in specific contexts or tasks)•This context-invariant coding could be a key, unique feature of human intelligence Rey et al. use a naturalistic memory task, in which subjects learn and then recall two different stories involving the same person in different contexts, while recording the activity of individual hippocampal neurons. They report similar single-neuron responses to the same identity in different contexts and tasks.