Learning and language in the unconscious human hippocampus.
Kalman A Katlowitz, Shraddha Shah, Melissa C Franch, Joshua Adkinson, James L Belanger, Raissa K Mathura, Domokos Meszéna, Elizabeth A Mickiewicz, Matthew McGinley, William Muñoz, Garrett P Banks, Sydney S Cash, Chih-Wei Hsu, Angelique C Paulk, Nicole R Provenza, Andrew Watrous, Ziv Williams, Sarah R Heilbronner, Robert Kim, Nuttida Rungratsameetaweemana, Benjamin Y Hayden, Sameer A Sheth
bioRxiv : the preprint server for biology April 9, 2025 preprint DOI: 10.1101/2025.04.09.648012 via PubMed
Summary
AI-generated from the abstractLearning, semantic processing, and online prediction persist in the human hippocampus during general anesthesia-induced loss of consciousness. Using high-density Neuropixels microelectrodes to record neural activity while playing tones to anesthetized patients, hippocampal neurons reliably detected oddball tones, and this effect grew over about ten minutes, consistent with learning. A recurrent neural network model showed that learning and oddball representation emerge from flexible tone discrimination. When language stimuli were played, single units and ensembles carried information about semantic and grammatical features of natural speech, even predicting semantic information about upcoming words. These results indicate that complex sensory processing occurs in the hippocampus even in the unconscious state.
Study at a glance
| Characteristics | Observational cohort |
|---|---|
| Population | Anesthetized patients |
| Intervention | general anesthesia |
| Duration | ∼10 minutes |
| Keywords | Neuroscience Brain research Consciousness Memory Anesthesia |
| Citations | 11 |
| Key finding | Hippocampal neurons reliably detect oddball tones and process semantic and grammatical features of speech during general anesthesia-induced loss of consciousness. |
Abstract
Consciousness is a fundamental component of cognition, 1 but the degree to which higher-order perception relies on it remains disputed. 2,3 Here we demonstrate the persistence of learning, semantic processing, and online prediction in individuals under general anesthesia-induced loss of consciousness. 4,5 Using high-density Neuropixels microelectrodes 6 to record neural activity in the human hippocampus while playing a series of tones to anesthetized patients, we found that hippocampal neurons could reliably detect oddball tones. This effect size grew over the course of the experiment (∼10 minutes), consistent with learning effects. A biologically plausible recurrent neural network model showed that learning and oddball representation are an emergent property of flexible tone discrimination. Last, when we played language stimuli, single units and ensembles carried information about the semantic and grammatical features of natural speech, even predicting semantic information about upcoming words. Together these results indicate that in the hippocampus, which is anatomically and functionally distant from primary sensory cortices, 7 complex processing of sensory stimuli occurs even in the unconscious state.