Precisely timed theta oscillations are selectively required during the encoding phase of memory

Brain oscillations have been hypothesized to support cognitive function by coordinating spike timing within and across brain regions, yet it is often not known when timing is either critical for neural computations or an epiphenomenon. The entorhinal cortex and hippocampus are necessary for learning...

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Published in:	Nature neuroscience Vol. 24; no. 11; pp. 1614 - 1627
Main Authors:	Quirk, Clare R., Zutshi, Ipshita, Srikanth, Sunandha, Fu, Maylin L., Devico Marciano, Naomie, Wright, Morgan K., Parsey, Darian F., Liu, Stanley, Siretskiy, Rachel E., Huynh, Tiffany L., Leutgeb, Jill K., Leutgeb, Stefan
Format:	Journal Article
Language:	English
Published:	New York Nature Publishing Group US 01-11-2021 Nature Publishing Group
Subjects:	631/378/1595/1636 631/378/3920 Activity patterns Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedical and Life Sciences Biomedicine Brain Brain research Cognitive ability Cortex (entorhinal) Entorhinal cortex Entorhinal Cortex - chemistry Entorhinal Cortex - physiology Entrainment Firing pattern Hippocampus Hippocampus (Brain) Hippocampus - chemistry Hippocampus - physiology Male Memory Memory - physiology Memory tasks Mental task performance Mice Mice, 129 Strain Mice, Transgenic Neural oscillations Neurobiology Neurosciences Optogenetics - methods Oscillations Pacemakers Parvalbumin Perturbation Physiological aspects Psychological aspects Short term memory Spatial Behavior - physiology Spatial memory Theta Rhythm - physiology Theta rhythms Time Factors United States
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Summary:	Brain oscillations have been hypothesized to support cognitive function by coordinating spike timing within and across brain regions, yet it is often not known when timing is either critical for neural computations or an epiphenomenon. The entorhinal cortex and hippocampus are necessary for learning and memory and exhibit prominent theta oscillations (6–9 Hz), which are controlled by pacemaker cells in the medial septal area. Here we show that entorhinal and hippocampal neuronal activity patterns were strongly entrained by rhythmic optical stimulation of parvalbumin-positive medial septal area neurons in mice. Despite strong entrainment, memory impairments in a spatial working memory task were not observed with pacing frequencies at or below the endogenous theta frequency and only emerged at frequencies ≥10 Hz, and specifically when pacing was targeted to maze segments where encoding occurs. Neural computations during the encoding phase were therefore selectively disrupted by perturbations of the timing of neuronal firing patterns. By manipulating the rhythmicity of neural activity in entorhinal cortex and hippocampus, Quirk et al. show that memory is impaired by aberrant oscillatory activity during the encoding phase, but not during retention or retrieval phases.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS These authors contributed equally to this work C.R.Q., I.Z., J.K.L., and S.Leutgeb conceived experiments, designed study, and interpreted data. C.R.Q., M.K.W., D.F.P., M.L.F., S.Liu, N.D.M., R.E.S., and T.L.H. collected data from the spatial alternation task and performed recordings in the open field. I.Z., C.R.Q., M.L.F., R.E.S., and T.L.H. performed recordings on the rectangular track. I.Z., C.R.Q., and S.Leutgeb analyzed single cell recording data, S.S. and S.Leutgeb analyzed LFP recording data, and C.R.Q. and S.Leutgeb analyzed behavior data. C.R.Q., I.Z., J.K.L., and S.Leutgeb prepared figures and wrote the manuscript. J.K.L., and S.Leutgeb managed the project.
ISSN:	1097-6256 1546-1726
DOI:	10.1038/s41593-021-00919-0