Plasticity and Language in the Anesthetized Human Hippocampus
Kalman A. KatlowitziD, Eric R. Cole, Elizabeth A. MickiewicziD, Shraddha ShahiD, Melissa C. FranchiD, Joshua A. AdkinsoniD, James L. Belanger, Raissa K. MathuraiD, Domokos MeszénaiD, Matthew J. McGinleyiD, William MuñoziD, Garrett P. BanksiD, Sydney S. CashiD, Chih‐Wei HsuiD, Angelique Christine PaulkiD, Nicole R. ProvenzaiD, Andrew J. WatrousiD, Ziv M. WilliamsiD, Alica M. GoldmaniD, Vaishnav KrishnaniD, Atul MaheshwariiD, Sarah R. HeilbronneriD, Robert KimiD, Nuttida RungratsameetaweemanaiD, Benjamin Y. HaydeniD, Sameer Anil ShethiD
Abstract
Consciousness is a fundamental component of cognition,1 but the degree to which higher-order pattern recognition relies on it remains disputed.2,3 Here we demonstrate the persistence of oddball discrimination, semantic processing, and online prediction in individuals under general anesthesia-induced loss of consciousness.4,5 Using high-density Neuropixels microelectrodes6 to record both single unit and local field potential neural activity in the human hippocampus while playing a series of tones to anesthetized patients, we found that hippocampal neurons and local oscillations retained some detection of oddball tones. This effect size grew over the course of the experiment ([~]10 minutes), demonstrating representational plasticity. A biologically plausible recurrent neural network model showed that learning and oddball representation are an emergent property of flexible tone discrimination. Moreover, when we played language stimuli, single units and local field potentials 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.
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