Abstract
Here, we reveal an unbiased view of the brain regions that provide specific inputs to aromatase-expressing cells in the medial amygdala, neurons that play an outsized role in the production of sex-specific social behaviors, using rabies tracing and light sheet microscopy. While the downstream projections from these cells are known, the specific inputs to the aromatase-expressing cells in the medial amygdala remained unknown. We observed established connections to the medial amygdala (e.g., bed nucleus of the stria terminalis and accessory olfactory bulb) indicating that aromatase neurons are a major target cell type for efferent input including from regions associated with parenting and aggression. We also identified novel and unexpected inputs from areas involved in metabolism, fear and anxiety, and memory and cognition. These results confirm the central role of the medial amygdala in sex-specific social recognition and social behavior, and point to an expanded role for its aromatase-expressing neurons in the integration of multiple sensory and homeostatic factors, which are likely used to modulate many other social behaviors.
Highlights
Social behaviors are necessary for communication, survival, and reproduction in species throughout the animal kingdom (Darwin, 1871; Marler, et al, 1979; Ueda et al, 2020), and depend on the integration of external and internal sensory cues
The full brain was digitally reconstructed and aligned to the Allen reference brain to allow 200 automated categorization by region. This approach allowed us to identify labeled neurons throughout the brain and to maintain the macroscopic organization of these cells (Figure 1C). 203 Population data: broad-scale brain regions 204 205 we identified the inputome for aromatase-expressing neurons located in the MeApd
We show that these neurons receive input from an unexpectedly wide range of regions, with strong inputs from regions linked to chemosensation, memory, metabolism, and the networks underlying social behaviors and decision-making. (Figure 10) 339 Two regions that are classically associated with the medial amygdala (MeA) are the accessory olfactory bulb (AOB) and bed nucleus of the stria terminalis (BNST) (Scalia, et al, 1975)
Summary
Social behaviors are necessary for communication, survival, and reproduction in species throughout the animal kingdom (Darwin, 1871; Marler, et al, 1979; Ueda et al, 2020), and depend on the integration of external and internal sensory cues. Chemosensory information, transduced by the main olfactory epithelium and the vomeronasal organ, provides the primary sensory input to a conserved network of brain regions dedicated to executing social behaviors (Newmann, et al, 1999). Social behaviors that are tightly associated with the MeA, including parenting, mate choice, and aggression, display clear sex differences (Chen, et al, 2020; Vochteloo, et al, 1987; Yao, et al, 2017). Each of these behaviors are critical for survival and reproduction. We use rabies-based circuit mapping in conjunction with whole-brain cleared tissue imaging to exhaustively characterize the sources of synaptic input to aromatase neurons in the MeA, and to identify the information channels that shape aromatase-dependent social behaviors. The Cyp19a1-Cre transgenic line was generated by BAC recombination (Yao et al, 2017); its expression pattern faithfully recapitulates endogenous aromatase expression (Yao et al, 2017) and displays no known behavioral deficits in either heterozygous or homozygous animals. 97 Viral injections: We used a retrograde tracing system based on the modified rabies virus (EnvA-SADΔG98 EGFP; Wickersham, et al, 2007) that uses two consecutive stereotaxic injections to visualize MeAarom+
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