Activity of hippocampal CA1 field neurons during aversive memory formation and reactivation in mice in vivo
- Authors: Roshchina M.A.1, Roshchin M.V.1, Borodinova A.A.1, Aseyev N.A.1, Zuzina A.B.1, Balaban P.M.1
-
Affiliations:
- Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
- Issue: Vol 18, No 4 (2023)
- Pages: 720-722
- Section: Conference proceedings
- URL: https://genescells.ru/2313-1829/article/view/623272
- DOI: https://doi.org/10.17816/gc623272
- ID: 623272
Cite item
Open Access
Access granted
Subscription or Fee Access
Abstract
According to modern concepts, the dorsal hippocampus, specifically the CA1 field, plays a crucial role in the formation and reactivation of contextual fear conditioning (CFC) memory [1–5]. However, the extent to which the neurons of the dorsal hippocampus participate in CFC learning or memory reactivation remains poorly understood. The aim of this study was to examine the in vivo activity of neurons in the hippocampal CA1 field during CFC memory training and testing. The study conducted experimentations on male mice of the C57Bl/6 line (N=4). Miniature fluorescence microscopes, also known as miniscopes, were used to monitor neuronal activity in the CA1 field. The CA1 field in the hippocampus was injected with an AAV vector carrying the GCaMP6s calcium sensor, and implanted with a GRIN lens in the same area as the miniscope lens. The mice underwent CFC task training and the duration of freezing was then measured.
After the training session, the mice exhibited a notable increase in freezing duration, suggesting the formation of context aversive memory. Throughout the training, a total of 591 active neurons were recorded (147.8±74.9 neurons per mouse), while 512 (128.0±40.6 neurons per mouse) neurons were recorded. The average frequency of calcium events per second during the complete duration of training session was 0.037±0.003, while for the testing, it was 0.042±0.015 events/second. Around 46% of the registered neurons remained active throughout the complete training procedure. The mean frequency of calcium events in these neurons surged considerably following the application of an electric shock (from 0.035±0.007 events/sec to 0.086±0.013 events/sec). Using k-means clustering, certain neurons showed increased activity after electric shock exposure, while others showed decreased activity. However, the type of activity change did not affect subsequent neuronal dynamics during memory retrieval. During memory retrieval, we observed that an average of 30–40% of neurons were reactivated. The number of active neurons notably decreased during episodes of freezing and almost all registered neurons were activated during episodes of movement. The average frequency of calcium events in the reactivating neurons did not change from the training to testing session.
Thus, new data was obtained on the activation of neurons in the hippocampal CA1 area during memory formation and retrieval in CFC.
Keywords
Full Text
According to modern concepts, the dorsal hippocampus, specifically the CA1 field, plays a crucial role in the formation and reactivation of contextual fear conditioning (CFC) memory [1–5]. However, the extent to which the neurons of the dorsal hippocampus participate in CFC learning or memory reactivation remains poorly understood. The aim of this study was to examine the in vivo activity of neurons in the hippocampal CA1 field during CFC memory training and testing. The study conducted experimentations on male mice of the C57Bl/6 line (N=4). Miniature fluorescence microscopes, also known as miniscopes, were used to monitor neuronal activity in the CA1 field. The CA1 field in the hippocampus was injected with an AAV vector carrying the GCaMP6s calcium sensor, and implanted with a GRIN lens in the same area as the miniscope lens. The mice underwent CFC task training and the duration of freezing was then measured.
After the training session, the mice exhibited a notable increase in freezing duration, suggesting the formation of context aversive memory. Throughout the training, a total of 591 active neurons were recorded (147.8±74.9 neurons per mouse), while 512 (128.0±40.6 neurons per mouse) neurons were recorded. The average frequency of calcium events per second during the complete duration of training session was 0.037±0.003, while for the testing, it was 0.042±0.015 events/second. Around 46% of the registered neurons remained active throughout the complete training procedure. The mean frequency of calcium events in these neurons surged considerably following the application of an electric shock (from 0.035±0.007 events/sec to 0.086±0.013 events/sec). Using k-means clustering, certain neurons showed increased activity after electric shock exposure, while others showed decreased activity. However, the type of activity change did not affect subsequent neuronal dynamics during memory retrieval. During memory retrieval, we observed that an average of 30–40% of neurons were reactivated. The number of active neurons notably decreased during episodes of freezing and almost all registered neurons were activated during episodes of movement. The average frequency of calcium events in the reactivating neurons did not change from the training to testing session.
Thus, new data was obtained on the activation of neurons in the hippocampal CA1 area during memory formation and retrieval in CFC.
About the authors
M. A. Roshchina
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
Email: lucky-a89@mail.ru
Russian Federation, Moscow
M. V. Roshchin
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
Email: lucky-a89@mail.ru
Russian Federation, Moscow
A. A. Borodinova
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
Email: lucky-a89@mail.ru
Russian Federation, Moscow
N. A. Aseyev
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
Email: lucky-a89@mail.ru
Russian Federation, Moscow
A. B. Zuzina
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
Author for correspondence.
Email: lucky-a89@mail.ru
Russian Federation, Moscow
P. M. Balaban
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences
Email: lucky-a89@mail.ru
Russian Federation, Moscow
References
- Holt W, Maren SJ. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. The Journal of Neuroscience. 1999;19(20):9054–9062. doi: 10.1523/JNEUROSCI.19-20-09054.1999
- Goshen I, Brodsky M, Prakash R, et al. Dynamics of retrieval strategies for remote memories. Cell. 2011;147(3):678–689. doi: 10.1016/j.cell.2011.09.033
- Reijmers LG, Perkins BL, Matsuo N, Mayford M. Localization of a stable neural correlate of associative memory. Science. 2007;317(5842):1230–1233. doi: 10.1126/science.1143839
- Liu X, Ramirez S, Pang PT, et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature. 2012;484(7394):381–385. doi: 10.1038/nature11028
- Tayler KK, Tanaka KZ, Reijmers LG, Wiltgen BJ. Reactivation of neural ensembles during the retrieval of recent and remote memory. Current Biology. 2013;23(2):99–106. doi: 10.1016/j.cub.2012.11.019
Supplementary files
