Social odor discrimination and its enhancement by associative learning in the hippocampal CA2 region

Hassan, Sami; Bigler, Shivani; Siegelbaum, S. A.

doi:10.1016/j.neuron.2023.04.026

Cited by 11 publications

(3 citation statements)

References 55 publications

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“…The complex mix of chemosensory signals embedded in rat urine convey information about a rat's social status and identity (Hurst, 2005). CA2 neurons differentially respond to urine from different conspecifics in mice (Hassan et al, 2023). The ability of CA2 to respond to social odors in the absence of conspecifics, as seen in our study, may allow rats to discern territory and identity information, which may drive social behavior even when other rats are not present.…”

Section: Discussionmentioning

confidence: 54%

Social odors drive hippocampal CA2 place cell responses to social stimuli

Robson,

Donahue,

Mably

et al. 2024

Preprint

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Hippocampal region CA2 is essential for social memory processing. Interaction with social stimuli induces changes in CA2 place cell firing during active exploration and sharp wave-ripples during rest following a social interaction. However, it is unknown whether these changes in firing patterns are caused by integration of multimodal social stimuli or by a specific sensory modality associated with a social interaction. Rodents rely heavily on chemosensory cues in the form of olfactory signals for social recognition processes. To determine the extent to which olfactory signals contribute to CA2 place cell responses to social stimuli, we recorded CA2 place cells in rats freely exploring environments containing social stimuli that included or lacked olfactory content. We found that CA2 place cell firing patterns significantly changed only when social odors were prominent. Also, place cells that increased their firing in the presence of social odors alone preferentially increased their firing during subsequent sharp wave-ripples. Our results suggest that olfactory cues are essential for changing CA2 place cell firing patterns during and after social interactions. These results support prior work suggesting CA2 performs social functions and shed light on processes underlying CA2 responses to social stimuli.

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Section: Discussionmentioning

confidence: 54%

Social odors drive hippocampal CA2 place cell responses to social stimuli

Robson,

Donahue,

Mably

et al. 2024

Preprint

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“…The lateral entorhinal cortex (LEC) relays such social olfactory information from the olfactory bulb and olfactory cortex to dCA2 through both a direct projection and an indirect path through the dentate gyrus to CA3 to CA2 trisynaptic circuit. Moreover, dCA2 is capable of discriminating the volatile social odors contained in urine from male mice 27 and silencing the direct LEC projection to dCA2 is sufficient to disrupt SNR memory 41 . Additionally, dCA2 receives modulatory projections from regions of the brain that relay social novelty cues, such as the supramammillary nucleus (SuM) 42 and the medial septum (MS) 43,44 .…”

Section: Discussionmentioning

confidence: 99%

“…Recent findings have provided insight into how dCA2 neural activity encodes conspecific identity and social novelty 24–26 . Furthermore, dCA2 has been found to incorporate both positive 27 and negative 28 valence associations into representations of social identity. However, an understanding of the specific neural mechanisms linking SNR memory and social aggression in dCA2 as either independent or complementary processes is lacking.…”

Section: Introductionmentioning

confidence: 99%

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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Cholinergic and behavior‐dependent beta and gamma waves are coupled between olfactory bulb and hippocampus

Leung,

Gill,

Shen

et al. 2024

Hippocampus

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Olfactory oscillations may enhance cognitive processing through coupling with beta (β, 15–30 Hz) and gamma (γ, 30–160 Hz) activity in the hippocampus (HPC). We hypothesize that coupling between olfactory bulb (OB) and HPC oscillations is increased by cholinergic activation in control rats and is reduced in kainic‐acid‐treated epileptic rats, a model of temporal lobe epilepsy. OB γ2 (63–100 Hz) power was higher during walking and immobility‐awake (IMM) compared to sleep, while γ1 (30–57 Hz) power was higher during grooming than other behavioral states. Muscarinic cholinergic agonist pilocarpine (25 mg/kg ip) with peripheral muscarinic blockade increased OB power and OB‐HPC coherence at β and γ1 frequency bands. A similar effect was found after physostigmine (0.5 mg/kg ip) but not scopolamine (10 mg/kg ip). Pilocarpine increased bicoherence and cross‐frequency coherence (CFC) between OB slow waves (SW, 1–5 Hz) and hippocampal β, γ1 and γ2 waves, with stronger coherence at CA1 alveus and CA3c than CA1 stratum radiatum. Bicoherence further revealed a nonlinear interaction of β waves in OB with β waves at the CA1‐alveus. Beta and γ1 waves in OB or HPC were segregated at one phase of the OB‐SW, opposite to the phase of γ2 and γ3 (100–160 Hz) waves, suggesting independent temporal processing of β/γ1 versus γ2/γ3 waves. At CA1 radiatum, kainic‐acid‐treated epileptic rats compared to control rats showed decreased theta power, theta‐β and theta‐γ2 CFC during baseline walking, decreased CFC of HPC SW with γ2 and γ3 waves during baseline IMM, and decreased coupling of OB SW with β and γ2 waves at CA1 alveus after pilocarpine. It is concluded that β and γ waves in the OB and HPC are modulated by a slow respiratory rhythm, in a cholinergic and behavior‐dependent manner, and OB‐HPC functional connectivity at β and γ frequencies may enhance cognitive functions.

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Social odor discrimination and its enhancement by associative learning in the hippocampal CA2 region

Cited by 11 publications

References 55 publications

Social odors drive hippocampal CA2 place cell responses to social stimuli

Social odors drive hippocampal CA2 place cell responses to social stimuli

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

Cholinergic and behavior‐dependent beta and gamma waves are coupled between olfactory bulb and hippocampus

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