UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice
Hippocampal ripples are transient population bursts that structure cortico-hippocampal communication and play a central role in memory processing. However, the mechanisms controlling ripple initiation in behaving animals remain poorly understood. Here we combine multisite extracellular and whole-cel...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2022-07-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/69596 |
| _version_ | 1811252411109474304 |
|---|---|
| author | Koichiro Kajikawa Brad K Hulse Athanassios G Siapas Evgueniy V Lubenov |
| author_facet | Koichiro Kajikawa Brad K Hulse Athanassios G Siapas Evgueniy V Lubenov |
| author_sort | Koichiro Kajikawa |
| collection | DOAJ |
| description | Hippocampal ripples are transient population bursts that structure cortico-hippocampal communication and play a central role in memory processing. However, the mechanisms controlling ripple initiation in behaving animals remain poorly understood. Here we combine multisite extracellular and whole-cell recordings in awake mice to contrast the brain state and ripple modulation of subthreshold dynamics across hippocampal subfields. We find that entorhinal input to the dentate gyrus (DG) exhibits UP and DOWN dynamics with ripples occurring exclusively in UP states. While elevated cortical input in UP states generates depolarization in DG and CA1, it produces persistent hyperpolarization in CA3 neurons. Furthermore, growing inhibition is evident in CA3 throughout the course of the ripple buildup, while DG and CA1 neurons exhibit depolarization transients 100 ms before and during ripples. These observations highlight the importance of CA3 inhibition for ripple generation, while pre-ripple responses indicate a long and orchestrated ripple initiation process in the awake state. |
| first_indexed | 2024-04-12T16:34:17Z |
| format | Article |
| id | doaj.art-eca976c5d51e410f977e2bbc854859f6 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:34:17Z |
| publishDate | 2022-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-eca976c5d51e410f977e2bbc854859f62022-12-22T03:25:03ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.69596UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake miceKoichiro Kajikawa0https://orcid.org/0000-0002-8626-4407Brad K Hulse1Athanassios G Siapas2https://orcid.org/0000-0001-8837-678XEvgueniy V Lubenov3https://orcid.org/0000-0002-1099-944XDivision of Biology and Biological Engineering, Division of Engineering and Applied Science, Computation and Neural Systems Program, California Institute of Technology, Pasadena, United StatesDivision of Biology and Biological Engineering, Division of Engineering and Applied Science, Computation and Neural Systems Program, California Institute of Technology, Pasadena, United StatesDivision of Biology and Biological Engineering, Division of Engineering and Applied Science, Computation and Neural Systems Program, California Institute of Technology, Pasadena, United StatesDivision of Biology and Biological Engineering, Division of Engineering and Applied Science, Computation and Neural Systems Program, California Institute of Technology, Pasadena, United StatesHippocampal ripples are transient population bursts that structure cortico-hippocampal communication and play a central role in memory processing. However, the mechanisms controlling ripple initiation in behaving animals remain poorly understood. Here we combine multisite extracellular and whole-cell recordings in awake mice to contrast the brain state and ripple modulation of subthreshold dynamics across hippocampal subfields. We find that entorhinal input to the dentate gyrus (DG) exhibits UP and DOWN dynamics with ripples occurring exclusively in UP states. While elevated cortical input in UP states generates depolarization in DG and CA1, it produces persistent hyperpolarization in CA3 neurons. Furthermore, growing inhibition is evident in CA3 throughout the course of the ripple buildup, while DG and CA1 neurons exhibit depolarization transients 100 ms before and during ripples. These observations highlight the importance of CA3 inhibition for ripple generation, while pre-ripple responses indicate a long and orchestrated ripple initiation process in the awake state.https://elifesciences.org/articles/69596rippleshippocampusinhibitionbrain stateswhole-cell |
| spellingShingle | Koichiro Kajikawa Brad K Hulse Athanassios G Siapas Evgueniy V Lubenov UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice eLife ripples hippocampus inhibition brain states whole-cell |
| title | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
| title_full | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
| title_fullStr | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
| title_full_unstemmed | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
| title_short | UP-DOWN states and ripples differentially modulate membrane potential dynamics across DG, CA3, and CA1 in awake mice |
| title_sort | up down states and ripples differentially modulate membrane potential dynamics across dg ca3 and ca1 in awake mice |
| topic | ripples hippocampus inhibition brain states whole-cell |
| url | https://elifesciences.org/articles/69596 |
| work_keys_str_mv | AT koichirokajikawa updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice AT bradkhulse updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice AT athanassiosgsiapas updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice AT evgueniyvlubenov updownstatesandripplesdifferentiallymodulatemembranepotentialdynamicsacrossdgca3andca1inawakemice |