Abstract
In the hippocampal circuit CA3 input plays a critical role in the organization of CA1 population activity, both during learning and sleep. While integrated spatial representations have been observed across the two hemispheres of CA1, these regions lack direct connectivity and thus the circuitry responsible remains largely unexplored. Here we investigate the role of CA3 in organizing bilateral CA1 activity by blocking synaptic transmission at CA3 terminals through the inducible transgenic expression of tetanus toxin. Although the properties of single place cells in CA1 were comparable bilaterally, we find a decrease of ripple synchronization between left and right CA1 after silencing CA3. Further, during both exploration and rest, CA1 neuronal ensemble activity is less coordinated across hemispheres. This included degradation of the replay of previously explored spatial paths in CA1 during rest, consistent with the idea that CA3 bilateral projections integrate activity between left and right hemispheres and orchestrate bilateral hippocampal coding.
Highlights
In the hippocampal circuit CA3 input plays a critical role in the organization of CA1 population activity, both during learning and sleep
We investigated the role of CA3 in organizing bilateral ensemble CA1 activity by genetically blocking synaptic transmission at CA3 terminals through the inducible transgenic expression of tetanus toxin (TeTX) and recording from bilateral CA1 in CA3-TeTX mice[5] and littermate controls (CTRs), as mice explored a familiar linear track, as well as during flanking periods of rest (Fig. 1a)
We compared the basic properties of place cells recorded in the left and right CA1 in CTR mice and in MUTs following the silencing of CA3 input, and found that the mean firing rate (FR) and spatial information (SI) during exploration were similar across hemispheres within both genotypes (FR: CTR L, 0.41 ± 0.036 Hz; CTR R, 0.39 ± 0.041 Hz; MUT L, 0.48 ± 0.040 Hz; MUT R, 0.44 ± 0.038 Hz; SI: CTR L, 0.87 ± 0.048 bits/spike; CTR R, 0.86 ± 0.055 bits/spike; MUT L, 0.70 ± 0.041 bits/spike; MUT R, 0.88 ± 0.063 bits/spike)
Summary
In the hippocampal circuit CA3 input plays a critical role in the organization of CA1 population activity, both during learning and sleep. The properties of single place cells in CA1 were comparable bilaterally, we find a decrease of ripple synchronization between left and right CA1 after silencing CA3 During both exploration and rest, CA1 neuronal ensemble activity is less coordinated across hemispheres. The properties of single place cells and SWRs in CA1 were comparable bilaterally, we observed a decrease of ripple synchronization between the left and right CA1 after silencing CA3. Cell assemblies, SWRs, and replay all endure following the chronic silencing of CA3 transmission, the properties of ensemble events were significantly altered, becoming poorer in quality and more lateralized These results suggest the CA3 output is important for the bilateral coordination of downstream CA1 spatial coding during spatial navigation and consolidation
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