Recognition memory via repetition suppression in mouse hippocampal dorsal CA2 pyramidal neurons expressing the vasopressin 1b receptor

Cymerblit‐Sabba, Adi; Stackmann, Michelle; Avram, Sarah K. Williams; Granovetter, Michael; Cliz, Nicholas I.; Pereira, Francisco; Smith, A. R.; Song, June; Lee, Heon-Jin; Young, W. Scott

doi:10.1101/2020.05.11.078915

Cited by 3 publications

(5 citation statements)

References 47 publications

(39 reference statements)

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“…Second, dCA2 activity is required for social novelty recognition (SNR) memory, the ability of a mouse to discriminate a novel from familiar conspecific 2,4 . And third, both electrophysiological 24,25 and cellular calcium imaging 26 studies have demonstrated that dCA2 neural activity discriminates a novel and familiar conspecific, with a higher rate of spike firing around a novel compared to familiar conspecific 24,34 .…”

Section: Discussionmentioning

confidence: 99%

“…Two potential mechanisms may account for how dCA2 activity in response to a novel animal may promote aggression. First, enhanced firing observed in dCA2 pyramidal neurons in the presence of a novel animal 24,34 may lead to increased output to the dLS, subsequently leading to greater disinhibition of VMHvl, thus triggering aggression. The second mechanism is based on results showing that a linear classifier can provide a generalized or abstract readout of novelty versus familiarity from the population level activity of dCA2 neurons 26 .…”

Section: Discussionmentioning

confidence: 99%

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Modulation of aggression by social novelty recognition memory in the hippocampal CA2 region

Villegas,

Siegelbaum

2024

Preprint

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The dorsal CA2 subregion (dCA2) of the hippocampus exerts a critical role in social novelty recognition (SNR) memory and in the promotion of social aggression. Whether the social aggression and SNR memory functions of dCA2 are related or represent independent processes is unknown. Here we investigated the hypotheses that an animal is more likely to attack a novel compared to familiar animal and that dCA2 promotes social aggression through its ability to discriminate between novel and familiar conspecifics. To test these ideas, we conducted a multi-day resident intruder (R-I) test of aggression towards novel and familiar conspecifics. We found that mice were more likely to attack a novel compared to familiarized intruder and that silencing of dCA2 caused a more profound inhibition of aggression towards a novel than familiarized intruder. To explore whether and how dCA2 pyramidal neurons encode aggression, we recorded their activity using microendoscopic calcium imaging throughout the days of the R-I test. We found that a fraction of dCA2 neurons were selectively activated or inhibited during exploration, dominance, and attack behaviors and that these signals were enhanced during interaction with a novel compared to familiarized conspecific. Based on dCA2 population activity, a set of binary linear classifiers accurately decoded whether an animal was engaged in each of these forms of social behavior. Of particular interest, the accuracy of decoding aggression was greater with novel compared to familiarized intruders, with significant cross-day decoding using the same familiar animal on each day but not for a familiar-novel pair. Together, these findings demonstrate that dCA2 integrates information about social novelty with signals of behavioral state to promote aggression towards novel conspecifics.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Modulation of aggression by social novelty recognition memory in the hippocampal CA2 region

Villegas,

Siegelbaum

2024

Preprint

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“…We focused on dCA2 because of its prominent role in the encoding, consolidation, and recall of social memory 4,5,7 . Previous studies using in vivo recordings found that dCA2 neurons respond during social interactions 10,11,23 and can distinguish between a novel and a familiar animal 10 . At the same time, CA2 neurons have been found to act as place cells, firing in particular regions of an environment either in the absence or presence of a conspecific, although CA2 place fields are less precise and stable than those of its CA1 and CA3 neighbors 9,10,21 .…”

Section: Discussionmentioning

confidence: 99%

Tuned geometries of hippocampal representations meet the demands of social memory

Boyle

Posani

Irfan

et al. 2022

Preprint

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Social recognition memory encompasses two distinct processes: familiarity - the ability to rapidly distinguish a novel from familiar individual - and recollection, the recall of detailed episodic memories of prior encounters with familiar individuals. Although it is clear that the hippocampus is important for different forms of episodic memory, including spatial memory and social recognition memory, whether and how neural activity in this single brain region may be able to encode both social familiarity and social recollection remains unclear. We addressed such questions using microendoscopic calcium imaging from pyramidal neurons in the dorsal CA2 region of the hippocampus (dCA2), an area crucial for social recognition memory that encodes social and spatial information, as mice explored novel and familiar conspecifics. Here we demonstrate that the geometry of dCA2 representations in neural activity space enables social familiarity, social identity, and spatial information to be readily disentangled. Importantly, highly familiar littermates were encoded in higher-dimensional neural representations compared to novel individuals. As a result of this coding strategy, dCA2 neural activity was able to both provide an abstract, low-dimensional representation of social familiarity that could readily distinguish a novel from familiar individual and encode detailed episodic memories associated with familiar individuals.

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Section: Introductionmentioning

confidence: 99%

“…The pyramidal neurons in CA2 co-express the vasopressin (Avp) 1b and oxytocin (Oxt) receptors (Avpr1b and Oxtr, respectively), through which the important neuropeptides, Avp and Oxt , carry their modulatory action on social cognition and social behavior [5][6][7] . Previously, we showed that loss of the Avpr1b from the pyramidal neurons of the CA2 results in inability of mice to recognize a familiar conspecific [6][7] . We also described an enhancement of social recognition following activation of the paraventricular nucleus (PVN) terminals in CA2, mediated by the Avpr1b 2 and, further, we were able to induce atypical partner preference behavior in mice through similar activation of the same neuronal pathway 8 .…”

Section: Introductionmentioning

confidence: 99%

Simultaneous Knockouts of the Oxytocin and Vasopressin 1b Receptors in Hippocampal CA2 Impair Social Memory

Cymerblit‐Sabba¹,

Walsh²,

Duan³

et al. 2023

Preprint

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Oxytocin (Oxt) and vasopressin (Avp) are two neuropeptides with many central actions related to social cognition. The oxytocin (Oxtr) and vasopressin 1b (Avpr1b) receptors are co-expressed in the pyramidal neurons of the hippocampal subfield CA2 and are known to play a critical role in social memory formation. How the neuropeptides perform this function in this region is not fully understood. Here, we report the behavioral effects of a life-long conditional removal (knockout, KO) of either the Oxtr alone or both Avpr1b and Oxtr from the pyramidal neurons of CA2 as well as the resultant changes in synaptic transmission within the different fields of the hippocampus. Surprisingly, the removal of both receptors results in mice that are unable to habituate to a familiar female presented for short duration over short intervals but are able to recognize and discriminate females when presented for a longer duration over a longer interval. Importantly, these double KO mice were unable to discriminate between a male littermate and a novel male. Synaptic transmission between CA3 and CA2 is enhanced in these mice, suggesting a compensatory mechanism is activated to make up for the loss of the receptors. Overall, our results demonstrate that co-expression of the receptors in CA2 is necessary to allow intact social memory processing.

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Recognition memory via repetition suppression in mouse hippocampal dorsal CA2 pyramidal neurons expressing the vasopressin 1b receptor

Cited by 3 publications

References 47 publications

Modulation of aggression by social novelty recognition memory in the hippocampal CA2 region

Modulation of aggression by social novelty recognition memory in the hippocampal CA2 region

Tuned geometries of hippocampal representations meet the demands of social memory

Simultaneous Knockouts of the Oxytocin and Vasopressin 1b Receptors in Hippocampal CA2 Impair Social Memory

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