Integrating pheromonal and spatial information in the amygdalo-hippocampal network

Villafranca-Faus, María; Vila-Martin, Manuel E.; Esteve, Daniel; Teruel-Sanchis, Anna; Cervera‐Ferri, Ana; Martínez‐Ricós, Joana; Lloret, Ana; Lanuza, Enrique; Teruel‐Martí, Vicent

doi:10.1038/s41467-021-25442-5

Cited by 14 publications

(20 citation statements)

References 52 publications

(81 reference statements)

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“…Hippocampal theta and gamma rhythms have been associated with novelty recognition (Penley et al, 2013;Kitanishi et al, 2015;Zheng et al, 2016;Brown et al, 2020;Kragel et al, 2020;Park et al, 2021;Wang et al, 2021). Since social stimuli have been shown to increase hippocampal theta and gamma oscillations (Tendler and Wagner, 2015;Villafranca-Faus et al, 2021;Brown et al, 2020) and mouse models of social dysfunction have been associated with alterations in hippocampal oscillations at both frequencies (Arbab et al, 2018;Aoki et al, 2017;Cheaha and Kumarnsit, 2015), we examined theta and gamma power in the vCA1 of WT and Shank3B KO mice in the presence of a novel mouse. Unexpectedly, we found no differences in either theta or gamma power in the absence of CA2 activation.…”

Section: Discussionmentioning

confidence: 99%

“…Because social stimuli have been shown to increase hippocampal theta power (Villafranca-Faus et al, 2021), and because chemogenetic activation of CA2 and the CA2-vCA1 pathway increased investigation of novel, but not familiar, mice (Figure 2E, 3E), we examined whether Shank3B KO CA2 DREADD-infected mice treated with CNO showed changes in vCA1 theta power during novel mouse exposure. We found that chemogenetic activation of the CA2 increased vCA1 theta power in the Shank3B KO DREADD virus group, but not in the WT groups (Figure 4C, Supplementary Table 1).…”

Section: Shank3b Ko Mice After Chemogenetic Activation Of the Ca2mentioning

confidence: 99%

“…The CA2 communicates with the vCA1 (Meira et al, 2019; Brown et al, 2020), which serves as the main hippocampal output carrying social memory information (Okuyama et al, 2016; Watarai et al, 2021). Social stimuli also increase CA1 oscillations in the gamma and theta ranges (Villafranca-Faus et al, 2021; Brown et al, 2020), and several animal models of social dysfunction exhibit abnormal hippocampal gamma and theta power (Aoki et al, 2017; Arbab et al, 2018; Modi et al, 2019). Taken together, these findings suggest that atypical SWRs, as well as gamma and theta rhythms, in the CA2-vCA1 pathway may contribute to social memory impairment.…”

Section: Introductionmentioning

confidence: 99%

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Activation of the CA2-vCA1 pathway reverses social discrimination dysfunction inShank3Bknockout mice

Cope

Wang

Waters

et al. 2022

Preprint

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Social memory dysfunction is a feature of several neuropsychiatric and neurodevelopmental disorders. Mutation or deletion of the SHANK3 gene, which codes for a synaptic scaffolding protein, has been linked to autism spectrum disorder (ASD) and Phelan-McDermid syndrome, conditions associated with impairments in social memory. Shank3B knockout (KO) mice exhibit several behavioral abnormalities that may be analogous to symptoms of ASD, including social discrimination deficits. The CA2 region of the hippocampus integrates numerous afferents and sends a major output to the ventral CA1 (vCA1), circuitry that plays an important role in social memory. Despite finding few differences in excitatory afferents to the CA2 in Shank3B KO mice, chemogenetic activation of CA2 excitatory neurons restored social recognition function to wildtype (WT) levels. Specific activation of the CA2-vCA1 circuitry had a similar effect. Neuronal oscillations in the theta, gamma and, sharp wave ripple ranges have been linked to social memory, but we observed no differences in these measures between WT and Shank3B KO mice in the vCA1 in response to social stimuli. However, activation of CA2 excitatory neurons enhanced vCA1 theta power in Shank3B KO mice, concurrent with behavioral improvements. These findings suggest that stimulating adult circuitry in a mouse model with neurodevelopmental impairments can be sufficient to invoke latent function, particularly with respect to social memory dysfunction. The extent to which vCA1 network oscillations in the theta range are responsible for rescued behavioral function remains unknown.

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Section: Discussionmentioning

confidence: 99%

Section: Shank3b Ko Mice After Chemogenetic Activation Of the Ca2mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Activation of the CA2-vCA1 pathway reverses social discrimination dysfunction inShank3Bknockout mice

Cope

Wang

Waters

et al. 2022

Preprint

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“…Part of the data from these experiments was published by Pardo-Bellver et al (2017) and Villafranca-Faus et al (2021). The surgical procedures, in vivo electrophysiological recordings, histological verification of the recording sites, preference test and behavioral analysis, and histological processing are thoroughly described in the aforementioned publications.…”

Section: Subjectsmentioning

confidence: 99%

Neural activity patterns in the chemosensory network encoding vomeronasal and olfactory information in mice

et al. 2022

Self Cite

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Rodents detect chemical information mainly through the olfactory and vomeronasal systems, which play complementary roles to orchestrate appropriate behavioral responses. To characterize the integration of chemosensory information, we have performed electrophysiological and c-Fos studies of the bulbo–amygdalar network in freely behaving female mice exploring neutral or conspecific stimuli. We hypothesize that processing conspecifics stimuli requires both chemosensory systems, and thus our results will show shared patterns of activity in olfactory and vomeronasal structures. Were the hypothesis not true, the activity of the vomeronasal structures would be independent of that of the main olfactory system. In the c-Fos analysis, we assessed the activation elicited by neutral olfactory or male stimuli in a broader network. Male urine induced a significantly higher activity in the vomeronasal system compared to that induced by a neutral odorant. Concerning the olfactory system, only the cortex–amygdala transition area showed significant activation. No differential c-Fos expression was found in the reward system and the basolateral amygdala. These functional patterns in the chemosensory circuitry reveal a strong top-down control of the amygdala over both olfactory bulbs, suggesting an active role of the amygdala in the integration of chemosensory information directing the activity of the bulbs during environmental exploration.

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“…The vomeronasal neurons are narrowly tuned sensory neurons that detect a range of small, natural ligands present in the exocrine secretions of conspecifics. The VNS is essential for the detection of both kairomones [ 13 , 14 ] and nonvolatile pheromones, which are involved in maternal recognition [ 15 ] and nonconscious sociosexual behaviors [ 16 , 17 ]. VNO neurons expressing the same vomeronasal receptor (VR) project axons to 10 to 30 distinct AOB glomeruli [ 18 , 19 ].…”

Section: Introductionmentioning

confidence: 99%

Neuroanatomical and Immunohistological Study of the Main and Accessory Olfactory Bulbs of the Meerkat (Suricata suricatta)

Torres

Ortiz‐Leal

Ferreiro³

et al. 2021

Animals

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We approached the study of the main (MOB) and accessory olfactory bulbs (AOB) of the meerkat (Suricata suricatta) aiming to fill important gaps in knowledge regarding the neuroanatomical basis of olfactory and pheromonal signal processing in this iconic species. Microdissection techniques were used to extract the olfactory bulbs. The samples were subjected to hematoxylin-eosin and Nissl stains, histochemical (Ulex europaeus agglutinin, Lycopersicon esculentum agglutinin) and immunohistochemical labelling (Gαo, Gαi2, calretinin, calbindin, olfactory marker protein, glial fibrillary acidic protein, microtubule-associated protein 2, SMI-32, growth-associated protein 43). Microscopically, the meerkat AOB lamination pattern is more defined than the dog’s, approaching that described in cats, with well-defined glomeruli and a wide mitral-plexiform layer, with scattered main cells and granular cells organized in clusters. The degree of lamination and development of the meerkat MOB suggests a macrosmatic mammalian species. Calcium-binding proteins allow for the discrimination of atypical glomerular subpopulations in the olfactory limbus between the MOB and AOB. Our observations support AOB functionality in the meerkat, indicating chemosensory specialization for the detection of pheromones, as identified by the characterization of the V1R vomeronasal receptor family and the apparent deterioration of the V2R receptor family.

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Integrating pheromonal and spatial information in the amygdalo-hippocampal network

Cited by 14 publications

References 52 publications

Activation of the CA2-vCA1 pathway reverses social discrimination dysfunction inShank3Bknockout mice

Activation of the CA2-vCA1 pathway reverses social discrimination dysfunction inShank3Bknockout mice

Neural activity patterns in the chemosensory network encoding vomeronasal and olfactory information in mice

Neuroanatomical and Immunohistological Study of the Main and Accessory Olfactory Bulbs of the Meerkat (Suricata suricatta)

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