Abstract
Innate social behaviours, such as mating and fighting, are fundamental to animal reproduction and survival1. However, social engagements can also put an individual at risk2. Little is known about the neural mechanisms that enable appropriate risk assessment and the suppression of hazardous social interactions. Here we identify the posteromedial nucleus of the cortical amygdala (COApm) as a locus required for the suppression of male mating when a female mouse is unhealthy. Using anatomical tracing, functional imaging and circuit-level epistatic analyses, we show that suppression of mating with an unhealthy female is mediated by the COApm projections onto the glutamatergic population of the medial amygdalar nucleus (MEA). We further show that the role of the COApm-to-MEA connection in regulating male mating behaviour relies on the neuromodulator thyrotropin-releasing hormone (TRH). TRH is expressed in the COApm, whereas the TRH receptor (TRHR) is found in the postsynaptic MEA glutamatergic neurons. Manipulating neural activity of TRH-expressing neurons in the COApm modulated male mating behaviour. In the MEA, activation of the TRHR pathway by ligand infusion inhibited mating even towards healthy female mice, whereas genetic ablation of TRHR facilitated mating with unhealthy individuals. In summary, we reveal a neural pathway that relies on the neuromodulator TRH to modulate social interactions according to the health status of the reciprocating individual. Individuals must balance the cost of social interactions relative to the benefit, as deficits in the ability to select healthy mates may lead to the spread of disease.
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Data availability
Source data are provided in the Supplementary Information. Sequencing data sets are publicly available in NCBI Gene Expression Omnibus (GEO) under accession GSE167176. All data are available from the corresponding author upon request.
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Acknowledgements
We thank N. Soares, M. Andina, K. Ronayne and I. D. Mejia for assistance with experiments; B. Noro and M. Trombly for critical reading of the manuscript; J. Huh for his contribution to the conceptual development of the project; B. Lowell for generously sharing the Trh-Cre mouse line; and H. Choi for the fibre photometry setup. This work was supported by the National Institute of Mental Health grants R01 MH122270 and R01 MH106497 (G.B.C.), the JPB Foundation (M.H. and G.B.C), Simons Center for the Social Brain Postdoctoral Fellowship (J.-T.K. and H.K.C.) and the Picower Fellows (J.-T.K. and H.L.).
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J.-T.K. and G.B.C. conceptualized the study. J.-T.K., H.L., C.R., M.H. and G.B.C. designed the experiments and/or provided advice and technical expertise. J.-T.K., H.L., C.R., A.S., J.F., D.H.C., S.B., H.A.S. and H.K.C. performed the experiments. I.R.W. provided reagents. J.-T.K. and G.B.C. wrote the manuscript with inputs from the co-authors.
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Extended data figures and tables
Extended Data Fig. 1 Male mice avoid mounting sick females.
a, b, Male mice were presented with a pair of oestrus female mice each injected intraperitoneally with either PBS (PBS female) or LPS (LPS female) (a). Mounting time during a 10-min test (b) (n = 9; from 2 independent experiments). c, Mounting time for male mice presented with two untreated, healthy females (n = 8; from 2 independent experiments). d, Investigation time of PBS and LPS females during a 10-min three-chamber assay (n = 5; from 2 independent experiments). e–i, These data are associated with Fig. 1a–e. Duration of other typical male behaviours while engaged in direct interactions with a PBS or LPS female (e, f). Percentage of individual female behaviours during males’ mounting attempts (g) and the number of cage crossings (h). Representative traces of male and female behaviours during direct interactions (i). **P < 0.01, ***P < 0.001 and ****P < 0.0001 calculated by paired two-tailed t-test (b), two-way ANOVA with Sidak’s post hoc test (f, g) and unpaired two-tailed t-test (h). Data are mean ± s.e.m. Pvalues are described in the Supplementary Statistical Information.
Extended Data Fig. 2 Role of the vomeronasal pathway in mounting behaviour.
a, Mounting time for males with a sham surgery (sham) or the VNO removed (VNOX) towards LPS females (sham, n = 5 and VNOX, n = 7; from 2 independent experiments). b–d, Virus encoding the anterograde trans-synaptic tracer (AAV1-hSyn-Cre) was targeted to the AOB in Ai14 reporter mice that express tdTomato in a Cre-dependent manner (b). Representative images (c) and quantification (d) of trans-synaptically labelled tdTomato+ neurons in BST, MEA and COApm at the specified anterior-posterior axis (n = 4; from 3 independent experiments). Scale bars, 500 μm. e–g, Virus encoding ChR2 (AAV2-hSyn-hChR2-eYFP) was targeted to the AOB (e, f). g, Representative image of FOS expression in the COApm upon photoactivation of the AOB, from n = 3 mice. Scale bars, 500 μm. h, These data are associated with Fig. 1g. Number of FOS-expressing neurons in the vomeronasal pathway after interaction with PBS or LPS females. **P < 0.01, ***P < 0.001 and ****P < 0.0001 calculated by unpaired two-tailed t-test (a), one-way ANOVA with Bonferroni’s post hoc test (d) and two-way ANOVA with Sidak’s post hoc test (h). Graph indicates mean ± s.e.m. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 3 Investigation of LPS females induces neural activity in the COApm of males.
a–c, These data are associated with Fig. 1h–o. a, Representative image of GCaMP6s expression in the COApm. Scale bar, 300 μm. b, Individual traces of COApm bulk fluorescence signal during interactions with a PBS or LPS female. c, Heat map of normalized COApm responses to PBS or LPS females. Each row represents a single investigation event. Investigation events were pooled from 6 mice from 3 independent experiments. Time = 0 indicates initiation of investigation. d, e, Virus encoding GCaMP6s (AAV1-Syn-GCaMP6s) was targeted to the COApm for fibre photometry recordings. Male mice were sequentially presented with an oestrus or dioestrus female in counterbalanced sessions. Representative traces of COApm bulk fluorescence signal (d) and the mean z-score of the fluorescence during direct investigation of the oestrus or dioestrus female (e) (oestrus, n = 5 and dioestrus, n = 5; from 3 independent experiments). f–j, Male mounting behaviours towards an oestrus or dioestrus, healthy female. Percentage of male mounting (f), mounting time (g), number of mounts (h), latency to mount (i) and percentage of female partners with mating plugs (j) (oestrus, n = 6 and dioestrus, n = 6; from 2 independent experiments). j, *P < 0.05 calculated by chi-square test of independence. Data are mean ± s.e.m. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 4 LPS odour suppresses male mating behaviours.
a–c, Male mice were presented with PBS or LPS odour (a). Representative images (b) and quantification (c) of FOS expression in the COApm of males after exposure to PBS or LPS odour (PBS odour, n = 6 and LPS odour, n = 8; from 2 independent experiments). Scale bar, 500 μm. d, e, Virus encoding GCaMP6s (AAV1-Syn-GCaMP6s) was targeted to the COApm for fibre photometry recordings. Male mice were sequentially presented with a PBS or LPS odour in counterbalanced sessions. Traces of COApm bulk fluorescence signal (solid line shows the average and shaded area indicates the s.e.m.) (d) and the mean z-score of the fluorescence during the first 20 s of direct investigation of the odour (e) (n = 6; from 3 independent experiments). f–m, Male mice were presented with a healthy female painted with PBS or LPS odour (f). Percentage of male mounting (g), mounting time (h), number of mounts (i), latency to mount (j) and duration of additional male behaviours while engaged in direct interactions with the female (k). Percentage of female behaviours in response to males’ mounting attempts (l) and the number of cage crossings (m) (PBS odour, n = 10 and LPS odour, n = 11; from 2 independent experiments). *P < 0.05, **P < 0.01 and ****P < 0.0001 calculated by unpaired two-tailed t-test (c, h–j), paired two-tailed t-test (e), chi-square test of independence (g) and two-way ANOVA with Sidak’s post hoc test (k). Data are mean ± s.e.m. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 5 COApm mediates suppression of mating behaviours towards unhealthy females.
a–d, These data are associated with Fig. 2a–e. a, Representative image of ChR2 expression in the COApm. b, Total direct investigation time of healthy females in the presence (ON) and absence (OFF) of COApm photoactivation. Duration of self grooming (c) and percentage of photoactivation trials with self grooming (d). Scale bar, 1 mm. e, f, These data are associated with Fig. 2i–m. Representative image of hM4Di expression in the COApm (e) and total direct investigation time of LPS females (f). Scale bar, 1 mm. g–k, Additional control experiments for data in Fig. 2i–m. Male mice expressing inhibitory DREADD (AAV2-hSyn-hM4D(Gi)-mCherry) in COApm were injected with either saline or CNO and tested for mounting behaviour towards LPS females (g). Percentage of male mounting (h), mounting time (i), number of mounts (j) and latency to mount (k) (saline, n = 8 and CNO, n = 7; from 2 independent experiments). l–p, Male mice expressing mCherry (AAV2-hSyn-mCherry) or inhibitory DREADD (hM4Di, AAV2-hSyn-hM4D(Gi)-mCherry) in COApm were injected with CNO and tested for mounting behaviour towards untreated, healthy oestrus females (l). Percentage of male mounting (m), mounting time (n), number of mounts (o) and latency to mount (p) (mCherry, n = 8 and hM4Di, n = 8; from 2 independent experiments). q–u, Male mice expressing inhibitory DREADD (AAV2-hSyn-hM4D(Gi)-mCherry) in COApm were injected with saline or CNO and tested for mounting behaviour towards untreated, healthy dioestrus females (q). Percentage of male mounting (r), mounting time (s), number of mounts (t), and latency to mount (u) (saline, n = 6 and CNO, n = 6; from 2 independent experiments). *P < 0.05, **P < 0.01 calculated by unpaired two-tailed t-test (c, i, j). Data are mean ± s.e.m. P values are described in the Supplementary Statistical Informatio.
Extended Data Fig. 6 COApm neurons preferentially project to MEA-Vglut2+ neurons.
a, b, Virus encoding the anterograde tracer (AAV2-hSyn-tdTomato) was targeted to the COApm. Total fluorescence intensity was measured in sub-regions receiving COApm axonal projections: MEA, BST, ventral hippocampus (HCv), lateral septum (LS), AOB and piriform cortex (PIR) (n = 4 mice; from 2 independent experiments). Scale bars, 500 μm. c, Virus encoding the anterograde trans-synaptic tracer (AAV1-hSyn-Cre) was targeted to the COApm of Ai14 reporter mice that express tdTomato in a Cre-dependent manner. Representative image of MEA post-synaptic neurons at AP −1.7 mm, from 3 independent experiments. Scale bar, 300 μm. d, mRNA expression of Vglut2 and Vgat in MEA (Image credit: Allen Institute). e–g, ChR2 (AAV2-hSyn-ChR2-eYFP) was targeted to the COApm (e). Representative images of ChR2 expression in COApm (f) and FOS expression in MEA upon photoactivation of COApm (g) (n = 3; from 2 independent experiments). Scale bars, 300 μm. h, i, Virus encoding GCaMP6s (AAV1-Syn-GCaMP6s) was targeted to the MEA of Vglut2-Cre mice for fibre photometry recordings. Male mice were sequentially presented with a PBS or LPS female in counterbalanced sessions. Representative traces of MEA-vGlut2+ bulk fluorescence signal (h) and the mean z-score of the fluorescence during direct investigation of the PBS or LPS female (i) (n = 3; from 2 independent experiments). i, *P < 0.05 calculated by paired two-tailed t-test. Data are mean ± s.e.m. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 7 COApm suppresses male mating behaviours by engaging MEA-Vglut2+ neurons.
These data are associated with Fig. 3f–i. Percentage of male mounting (a–d), number of mounts (e–h), latency to mount (i–l). Representative images of ChR2 expression in COApm (m) and hM4Di expression in MEA (n) of Vglut2-Cre mice with concurrent photoactivation of COApm-MEA projections and hM4Di-inhibition of MEA-Vglut2+ neurons. Scale bars, 500 μm. *P < 0.05, **P < 0.01, ***P < 0.001 and ****P < 0.0001 calculated by chi-square test of independence (a–c) and unpaired two-tailed t-test (e–k). Data are mean ± s.e.m. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 8 Summary of gene-expression profiling in COApm neurons projecting to MEA-Vglut2+ neurons.
a, A combination of AAV1-Syn-FLEX-TTA and AAV-TRE-B19G, and RV∆G-L10a-eGFP were sequentially injected into the MEA of Vglut2-Cre mice to express L10a-eGFP in COApm neurons projecting to MEA-Vglut2+ neurons (COApm-proj). COApm tissue was collected and immediately used for TRAP analyses. Control mice were injected with AAV.PHP.eB-Syn-L10a-eGFP via retro-orbital injection in order to label COApm neurons with L10a-eGFP independently of their efferent projections (Total COApm). b, Volcano plot showing log2-fold change plotted against −log10 FDR for the labelled COApm neurons projecting to the MEA-Vglut2+ population (COApm-Proj.) compared to the total COApm. Differentially expressed genes that pass the threshold for the FDR are highlighted in red. c, Heat map showing COApm-differentially expressed genes that belong to the KEGG neuroactive ligand–receptor interaction pathway. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 9 COApm-TRH+ neurons mediate the suppression of male mating towards unhealthy females.
a–g, Trh-Cre male mice expressing tdTomato (AAV1/2-Ef1α-DO-DIO-tdTomato(tdT)-eGFP, Control) or ChR2 (AAV1/2-Ef1α-DO-ChR2-mCherry, ChR2) in Cre− neurons were tested for mating behaviours towards healthy females with COApm photoactivation (a). Representative images (b) and quantification (c) of FOS expression in COApm. Percentage of male mounting (d), mounting time (e), number of mounts (f), and latency to mount (g) with photoactivation of COApm-TRH− cells (control, n = 5 and ChR2, n = 5; from 2 independent experiments). Scale bars, 500 μm. h–l, Calcium imaging of MEA brain slices from Vglut2-Cre mice expressing GCaMP7f (AAV1-hSyn-FLEX-GCaMP7f) in MEA-Vglut2+ neurons upon taltirelin (10 μM) application (h). i, Representative images of MEA slices before (−15 s) and after (+35 s) taltirelin application. Example traces of fluorescence signal from individual neurons (j) and the average of the fluorescence signal (solid line shows average and shaded area represents the s.e.m.) (k) upon taltirelin application. l, Area under the curve (AUC) of the average fluorescence signal from individual MEA slices binned every 30 s (n = 6 slices, from 3 mice). Scale bars, 50 μm. m, These data are associated with Fig. 4k–o. Total duration of direct investigation following microinjection of the TRH analogue taltirelin into MEA. *P < 0.05, **P < 0.01 and ***P < 0.001 calculated by unpaired two-tailed t-test (c, m) and Friedman test with Dunn’s multiple comparisons test (l). Data are mean ± s.e.m. P values are described in the Supplementary Statistical Information.
Extended Data Fig. 10 Suppression of mating engages TRH–TRHR signalling in the COApm-MEA projection.
a, Schematic depicting the targeting construct used to generate the Trhr conditional-knockout mouse line. b, c, Representative images (AP −1.8 mm) (b) and quantification (c) of Trhr mRNA expression in the MEApv of Trhrfl/fl mice with or without Cre expression (AAV1-hSyn-Cre) (Trhrfl/fl, n = 3 and Trhrfl/fl with Cre, n = 3; from 2 independent experiments). Scale bars, 20 μm. d–g, In vivo recordings of MEA responses to COApm inputs in Trhr conditional-knockout mice. Trhrfl/fl mice were injected with AAV2-hSyn-ChR2-eYFP in COApm and either AAV1-hSyn-GFP (GFP) or AAV1-hSyn-Cre (Cre) in MEApv. d, Local field potentials evoked by a 10-ms photoactivation were recorded from MEApv in anaesthetized mice using an optrode. e, Representative image of electrode localization. Representative waveforms (f) and amplitudes (baseline-to-negative peak) of MEApv responses evoked by photoactivation of COApm inputs (g) (GFP, n = 6 and Cre, n = 6; from 6 independent experiments). Scale bar, 300 μm. ***P < 0.001 and ****P < 0.0001 calculated by unpaired two-tailed t-test (c, g). Data are mean ± s.e.m. P values are described in the Supplementary Statistical Information.
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Kwon, JT., Ryu, C., Lee, H. et al. An amygdala circuit that suppresses social engagement. Nature 593, 114–118 (2021). https://doi.org/10.1038/s41586-021-03413-6
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DOI: https://doi.org/10.1038/s41586-021-03413-6
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