Volitional learning promotes theta phase coding in the human hippocampus

Electrophysiological studies in rodents show that active navigation enhances hippocampal theta oscillations (4-12 Hz), providing a temporal framework for stimulus-related neural codes. Here we show that active learning promotes a similar phase coding regime in humans, although in a lower frequency r...

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Detalles Bibliográficos
Autores: Pacheco Estefan, Daniel|||0000-0003-2253-5172, Zucca, Riccardo|||0000-0003-4808-6010, Arsiwalla, Xerxes D., Principe, Alessandro, Zhang, Hui, Rocamora Zúñiga, Rodrigo Alberto|||0000-0001-7345-4300, Axmacher, Nikolai|||0000-0002-0475-6492, Verschure, Paul F. M. J.
Tipo de recurso: artículo
Fecha de publicación:2021
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:322710
Acceso en línea:https://ddd.uab.cat/record/322710
https://dx.doi.org/urn:doi:10.1073/pnas.2021238118
Access Level:acceso abierto
Palabra clave:active learning
intracranial EEG
theta oscillations
neural phase coding
hippocampus
Descripción
Sumario:Electrophysiological studies in rodents show that active navigation enhances hippocampal theta oscillations (4-12 Hz), providing a temporal framework for stimulus-related neural codes. Here we show that active learning promotes a similar phase coding regime in humans, although in a lower frequency range (3-8 Hz). We analyzed intracranial electroencephalography (iEEG) from epilepsy patients who studied images under either volitional or passive learning conditions. Active learning increased memory performance and hippocampal theta oscillations and promoted a more accurate reactivation of stimulus-specific information during memory retrieval. Representational signals were clustered to opposite phases of the theta cycle during encoding and retrieval. Critically, during active but not passive learning, the temporal structure of intracycle reactivations in theta reflected the semantic similarity of stimuli, segregating conceptually similar items into more distant theta phases. Taken together, these results demonstrate a multilayered mechanism by which active learning improves memory via a phylogenetically old phase coding scheme.