Abstract
The nonapeptide system modulates numerous social behaviors through oxytocin and vasopressin activation of the oxytocin receptor (OXTR) and vasopressin receptor (AVPR1A) in the brain. OXTRs and AVPR1As are widely distributed throughout the brain and binding densities exhibit substantial variation within and across species. Although OXTR and AVPR1A binding distributions have been mapped for several rodents, this system has yet to be characterized in the spiny mouse (Acomys cahirinus). Here we conducted receptor autoradiography and in situ hybridization to map distributions of OXTR and AVPR1A binding and Oxtr and Avpr1a mRNA expression throughout the basal forebrain and midbrain of male and female spiny mice. We found that nonapeptide receptor mRNA is diffuse throughout the forebrain and midbrain and does not always align with OXTR and AVPR1A binding. Analyses of sex differences in brain regions involved in social behavior and reward revealed that males exhibit higher OXTR binding densities in the lateral septum, bed nucleus of the stria terminalis, and anterior hypothalamus. However, no association with gonadal sex was observed for AVPR1A binding. Hierarchical clustering analysis further revealed that co-expression patterns of OXTR and AVPR1A binding across brain regions involved in social behavior and reward differ between males and females. These findings provide mapping distributions and sex differences in nonapeptide receptors in spiny mice. Spiny mice are an excellent organism for studying grouping behaviors such as cooperation and prosociality, and the nonapeptide receptor mapping here can inform the study of nonapeptide-mediated behavior in a highly social, large group-living rodent.
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Data availability
Data are available upon request from the corresponding author.
Abbreviations
- AOB:
-
Accessory olfactory bulb
- aco:
-
Anterior commissure
- AI:
-
Agranular insular area of the cortex
- AHAL:
-
Amygdalohippocampal area, anterolateral part
- AH:
-
Anterior hypothalamus
- AOA:
-
Anterior olfactory areas
- APT:
-
Anterior pretectal nucleus
- BLA:
-
Basolateral amygdala
- BNST:
-
Bed nucleus of the stria terminalis
- BNSTa:
-
Bed nucleus of the stria terminalis, anterior division
- BNSTp:
-
Bed nucleus of the stria terminalis, posterior division
- CPu:
-
Caudate putamen
- CeA:
-
Central amygdala
- Cg:
-
Cingulate cortex
- cc:
-
Corpus callosum
- Cg2:
-
Cortical layer 2
- Cg5:
-
Cortical layer 5
- DG:
-
Dentate gyrus
- VDB:
-
Diagonal band nucleus
- DI:
-
Dysgranular insular cortex
- GP:
-
Globus pallidus
- Hi:
-
Hippocampus
- CA1:
-
Hippocampal field CA1
- CA1py:
-
Hippocampal field CA1 pyramidal layer
- CA3:
-
Hippocampal field CA3
- IP:
-
Interpeduncular nucleus
- LD:
-
Lateral dorsal nucleus of thalamus
- LH:
-
Lateral hypothalamus
- LS:
-
Lateral septum
- LSc:
-
Lateral septum, caudo-dorsal region
- LSv:
-
Lateral septum, ventral region
- MOB:
-
Main olfactory bulb
- MOBgl:
-
Main olfactory bulb, glomerular layer
- MOBgr:
-
Main olfactory bulb, granule layer
- MeA:
-
Medial amygdala
- MG:
-
Medial geniculate nucleus of the thalamus
- MM:
-
Medial mammillary nucleus of the hypothalamus
- MPOA:
-
Medial preoptic area of the hypothalamus
- NAcc:
-
Nucleus accumbens
- OT:
-
Olfactory tubercle
- och:
-
Optic chiasm
- PV:
-
Paraventricular thalamic nucleus
- PVA:
-
Paraventricular thalamic nucleus, anterior division
- PAG:
-
Periaqueductal gray
- PVG:
-
Periventricular gray
- PIR:
-
Piriform area
- Re:
-
Reuniens thalamic nucleus
- SC:
-
Superior colliculus
- SuG:
-
Superior colliculus, superficial gray, sensory related
- SCm:
-
Superior colliculus, motor related
- SCN:
-
Suprachiasmatic nucleus of the hypothalamus
- TT:
-
Taenia tecta
- 3 V:
-
Third ventricle
- VPL:
-
Ventral posterolateral nucleus of the thalamus
- VMH:
-
Ventromedial hypothalamic nucleus
- VPall:
-
Ventral pallidum
- VIS:
-
Visual areas of the cortex
- ZI:
-
Zona incerta
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Funding
We would like to acknowledge funding from the Esther A. and Joseph Klingenstein Fund (Klingenstein-Simons Fellowship Award in Neuroscience to AMK), the National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR070313 to AWS), the National Science Foundation (IOS-1353713 to AWS), and the National Institute of Mental Health (Emory CONTE Center Pilot Project Grant; P50MH100023 to LJY and P51OD11132 to Emory National Primate Research Center).
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JMP cryosectioned brains, conducted in situ hybridization, quantified receptor binding and mRNA expression, and wrote the manuscript. KI conducted the competitive binding assays and receptor autoradiography. KJW analyzed the data. AWS provided feedback on and edited the manuscript. LJY designed the study, provided feedback on and edited the manuscript, and acquired funding. AMK designed the study, analyzed the data, wrote the manuscript, and acquired funding.
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All procedures were approved by the Institutional Animal Care and Use Committee of Emory University.
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Powell, J.M., Inoue, K., Wallace, K.J. et al. Distribution of vasopressin 1a and oxytocin receptor protein and mRNA in the basal forebrain and midbrain of the spiny mouse (Acomys cahirinus). Brain Struct Funct 228, 413–431 (2023). https://doi.org/10.1007/s00429-022-02581-z
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DOI: https://doi.org/10.1007/s00429-022-02581-z