Abstract
The ability to remember conspecifics is critical for adaptive cognitive functioning and social communication, and impairments of this ability are hallmarks of autism spectrum disorders (ASDs). Although hippocampal ventral CA1 (vCA1) neurons are known to store social memories, how their activities are coordinated remains unclear. Here we show that vCA1 social memory neurons, characterized by enhanced activity in response to memorized individuals, were preferentially reactivated during sharp-wave ripples (SPW-Rs). Spike sequences of these social replays reflected the temporal orders of neuronal activities within theta cycles during social experiences. In ASD model Shank3 knockout mice, the proportion of social memory neurons was reduced, and neuronal ensemble spike sequences during SPW-Rs were disrupted, which correlated with impaired discriminatory social behavior. These results suggest that SPW-R-mediated sequential reactivation of neuronal ensembles is a canonical mechanism for coordinating hippocampus-dependent social memories and its disruption underlie the pathophysiology of social memory defects associated with ASD.
Highlights
The ability to recognize and memorize familiar conspecifics is crucial for animals that engage in social interactions [1, 2]
The subject and a stimulator mouse were left in the home cage for 2 h of familiarization, which has been shown to be a sufficient amount of time for the emergence of both memory-dependent social discriminatory behavior and social memory neurons in the ventral CA1 sub-region of the hippocampus (vCA1) [5]
A recent study reported that dorsal CA2 (dCA2) neurons respond to novel conspecifics during social interaction zone (Fig. 1j), indicates that some vCA1 social social interaction and are reactivated during sharp-wave ripples (SPW-Rs) [40]
Summary
The ability to recognize and memorize familiar conspecifics is crucial for animals that engage in social interactions [1, 2]. The ventral CA1 sub-region of the hippocampus (vCA1) contains neurons that respond to other individuals [5] but not to inanimate objects [6] and has been identified as a key locus for social memory storage [5, 7]. Hippocampal sharp-wave ripples (SPW-Rs) are transient, highfrequency, field oscillations that are typically observed during slowwave sleep and quiet wakefulness [8] and play a pivotal role in the formation of episodic memories encoded in the hippocampus. The SPW-Rs that arise in the ventral segment of the hippocampus often remain isolated [17]. It remains unclear whether the ventral hippocampus neuronal activity during SPW-Rs inherently represents spatial information or is used for processing related to other aspects, such as social information
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