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Galanin neurons in the medial preoptic area govern parental behaviour

Nature volume 509, pages 325–330 (2014)Cite this article

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Abstract

Mice display robust, stereotyped behaviours towards pups: virgin males typically attack pups, whereas virgin females and sexually experienced males and females display parental care. Here we show that virgin males genetically impaired in vomeronasal sensing do not attack pups and are parental. Furthermore, we uncover a subset of galanin-expressing neurons in the medial preoptic area (MPOA) that are specifically activated during male and female parenting, and a different subpopulation that is activated during mating. Genetic ablation of MPOA galanin neurons results in marked impairment of parental responses in males and females and affects male mating. Optogenetic activation of these neurons in virgin males suppresses inter-male and pup-directed aggression and induces pup grooming. Thus, MPOA galanin neurons emerge as an essential regulatory node of male and female parenting behaviour and other social responses. These results provide an entry point to a circuit-level dissection of parental behaviour and its modulation by social experience.

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Figure 1: Pup-directed behaviour of Trpc2−/− and Trpc2+/− virgin animals and switch from attack to parenting in males after mating.
Figure 2: Parenting activates galanin-expressing neurons in the MPOA.
Figure 3: Ablation of MPOA Gal+ neurons impairs maternal behaviour in virgin females.
Figure 4: Ablation of MPOA Gal+ neurons impairs paternal behaviour in fathers.
Figure 5: Optogenetic activation of MPOA Gal+ neurons in males suppresses attack and promotes pup grooming.

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Acknowledgements

We thank K. Deisseroth for the Cre-dependent AAV-ChR2:EYFP construct; E. Boyden for the Cre-dependent AAV-GFP construct; N. Shah for the AAV-Flex-taCasp3-TEVp virus; S. Sullivan for behaviour annotation and scoring; R. Hellmiss for figure artwork; E. Soucy and J. Greenwood for technical assistance. We also thank members of the Dulac and Uchida laboratories and V. Murthy, A. Schier and M. Meister for advice on experiments and statistical analysis and comments on the manuscript, and the anonymous reviewers for their helpful suggestions and comments. This work was supported by the Howard Hughes Medical Institute and the National Institute of Health (NIDCD).

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Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Howard Hughes Medical Institute, Center for Brain Science, Harvard University, Cambridge, 02138, Massachusetts, USA

    Zheng Wu, Anita E. Autry, Joseph F. Bergan & Catherine G. Dulac

  2. Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, 02138, Massachusetts, USA

    Mitsuko Watabe-Uchida

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Contributions

Z.W. and C.G.D. conceived and designed the study. Z.W. and A.E.A. performed the experiments and collected the data. J.F.B. and Z.W. developed the setup for ChR2-mediated cell activation. M.W.-U. constructed the AAV-DTA virus. Z.W. and C.G.D. interpreted the results and wrote the paper with comments from A.E.A., J.F.B. and M.W.-U.

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Correspondence to Catherine G. Dulac.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Identification of Gal as a marker for cells involved in parenting and characterization of MPOA Gal+ cells.

a, Enrichment ratio of markers in parenting induced MPOA c-fos in virgin females. The enrichment ratio of a given marker is calculated as the percentage of the c-fos+ cells co-expressing the marker, divided by the percentage of NeuN+ cells co-expressing this marker. b, The percentages of parenting induced MPOA c-fos+ cells co-expressing markers and the percentages of marker cells co-expressing c-fos. c, Percentages of Gal+ cells in the MPOA in virgin and sexually experienced males and females fail to identify any sexual dimorphism in MPOA Gal+ cell representation. Mean + s.e.m., one-way ANOVA, P > 0.2. d, Fold increase of Gal mRNA in situ staining intensity compared to background in virgin females, virgin males and fathers. Gal mRNA expression is slightly higher (10% increase) in females than in males. Mean + s.e.m., one-way ANOVA, ***P < 0.001, NS, not significant. e, f, Percentages of c-fos+ cells co-expressing Gad1 in fathers and virgin females. ND, not determined. Mean + s.e.m., t-test, **P < 0.01. g, h, Percentages of Gal+ cells co-expressing Gad1 in virgin males, fathers and virgin females. Mean + s.e.m., one-way ANOVA, P > 0.1.

Extended Data Figure 2 Targeted Gal+ cell ablation in the MPOA.

a, Co-labelling of Gal and Cre expressing cells by mRNA in situ hybridization in Gal-Cre females indicates near perfect overlap. b, Schematic map of the Cre-dependent AAV-DTA virus; DTA is doubly flanked by two sets of incompatible lox sites and inverted to enable transcription after Cre-mediated recombination. c, Gal mRNA expression in the MPOA of ablated and control males. d, Number of MPOA Gal+ cells in ablation group compared to controls. Mean + s.e.m., t-test, ***P < 0.001. e, Number of MPOA Trh+ cells in the ablation group and control. Mean + s.e.m., t-test, P > 0.2. f–h, Gal+ cell numbers in the AVPe (f), anterior part of the PVN (g) and the DMH (h) in MPOA targeted ablation compared to control. Mean + s.e.m., t-test, P > 0.1.

Extended Data Figure 3 Females with MPOA Gal+ cell ablation compared to Gal-Cre+ controls injected with AAV-Flex-GFP.

a, Behaviour of MPOA Gal+ cell ablated virgin females with over 50% ablation efficiency (n = 15) compared to Gal-Cre+ controls injected with AAV-Flex-GFP (n = 13). Chi-square test, P < 0.05. b, Percentage of pups retrieved by Gal+ cell ablated virgin females as a function of time compared to the controls. The retrieving data of the two pups in each test are combined. Kolmogorov–Smirnov test, P < 0.05. c–f, Crouching (c), pup grooming (d), nest building (e) and maternal interaction (f) in the Gal+ cell ablated virgin females and control. Mean ± s.e.m. Mann–Whitney test, *P < 0.05, **P < 0.01, ***P < 0.001. The control females with the longest crouching and of nest building duration are different individuals.

Extended Data Figure 4 Deficits in retrieving behaviour of mothers with MPOA Gal+ cell ablation.

a, Behaviour of MPOA Gal+ cell ablated mothers (n = 8) compared to controls (n = 8). Fisher’s exact test, P < 0.05. b, Number of pups retrieved by each mother. Mean ± s.e.m. Mann–Whitney test, *P < 0.05. c, Percentage of pups retrieved by the ablation group as a function of time compared to the controls. The retrieving data of the four pups in each test are combined. Kolmogorov–Smirnov test, P < 0.001.

Extended Data Figure 5 Mating, inter-male aggression and locomotor activity of MPOA Gal+ cell ablated fathers.

a-c, Locomotor behaviour of MPOA Gal+ cell ablated and control fathers in a 5 min test in an open arena, measuring the distance moved (a), time spent in the centre zone (b) and the average velocity (c). Mean + s.e.m., t-test, P > 0.3. d–f, Inter-male aggression of MPOA Gal+ cell ablated and control fathers, measuring duration of attack (d), latency to attack (e) and duration of grooming the intruder (f). Mean ± s.e.m. Mann–Whitney test, P > 0.2. g–i, Duration of mounting (g), latency to mount (h) and duration of mounting with pelvic thrust (i) of MPOA Gal+ cell ablated fathers compared to controls. Mean ± s.e.m. Mann–Whitney test, *P < 0.05.

Extended Data Figure 6 Parenting, mating and inter-male aggression of MPOA Th+ cell ablated fathers.

a, Th mRNA expression in the MPOA of Th+ cell ablated and control fathers. b, Number of MPOA Th+ cells in ablation group compared to controls. Mean + s.e.m., t-test, ***P < 0.001. c, Number of AVPe Th+ cells in MPOA targeted ablation. Mean + s.e.m., t-test, P = 0.07. d, The number of MPOA Th+ cell loss compared to the Gal+ cell ablation experiments. One male had a failed Th+ cell ablation and was removed from the data set hereafter. The Th+ cell loss is ∼87% of the Gal+ cell loss. e, Behaviour type of MPOA Th+ cell ablated fathers compared to controls. Fisher’s exact test, P > 0.6. f, Combined percentage of pups (out of two) retrieved by the Th+ cell ablation group as a function of time compared to the controls. Kolmogorov–Smirnov test, P > 0.9. g–i, Crouching (g), pup grooming (h) and nest building (i) in the Th+ cell ablated fathers and control. Mean ± s.e.m. Mann–Whitney test, P > 0.2. The control male with the longest pup grooming also has the longest nest building activity, but not the longest duration of crouching. j–l, Duration of mounting (j), latency to mount (k) and duration of mounting with pelvic thrust (l) of MPOA Th+ cell ablated males compared to control in a mating assay. Mean ± s.e.m. Mann–Whitney test, P > 0.3. m–o, Duration of attack (m), latency to attack (n) and duration of grooming the intruder (o) in MPOA Th+ cell ablated males compared to control in an inter-male aggression assay. Mean ± s.e.m. Mann–Whitney test, P > 0.3.

Extended Data Figure 7 Behaviour raster plot of Gal::ChR2 and control virgin males with and without light illumination.

Each row represents a single trial lasting for 5 min or until the male attacked the pup. Trials are grouped by experiment conditions and sorted by trial length. Roman numerals indicate the sample trials shown in Fig. 5f. Various elements of the behaviour are colour coded and labelled in the insert.

Extended Data Figure 8 Behaviour raster plot of mated Gal::ChR2 and control males with and without light illumination.

Each row represents a 10-min trial. Trials are grouped by experiment conditions. Roman numerals indicate the sample trials shown in Fig. 5i. Various elements of the behaviour are colour coded and labelled in the insert.

Extended Data Figure 9 Mating, inter-male aggression and locomotor activity of virgin males with MPOA Gal+ cell activation and controls of light stimulation and viral infection.

a–c, Duration of mounting (a), latency to mount (b) and duration of mounting with pelvic thrust (c) in virgin males with Gal+ cell activation compared to controls in a mating assay. Paired t-test, P > 0.7. d–f, Duration of attack (d), latency to attack (e) and duration of grooming the intruder (f) in virgin males with Gal+ cell activation compared to controls in an inter-male aggression assay. Paired t-test, *P < 0.05, NS. not significant. g, Distance moved in virgin males with Gal+ cell activation compared to controls. Paired t-test, ***P < 0.001. h, i, Time spent sniffing the intruder in mating (h) and inter-male aggression (i) assay. Paired t-test, P > 0.6. j, The duration of light stimulation in each behaviour test as a percentage of the total trial length. Mean + s.e.m., one-way ANOVA, P > 0.6. k, The percentages of Gal+ and Gal+/c-fos+ cells co-expressing fluorescent protein, in females injected with AAV5-Flex-ChR2-EYFP or AAV8-Flex-GFP after maternal interaction with pups. Mean + s.e.m., two-way ANOVA examining the differences in the infection of the two viruses and the two cell populations, P > 0.2 for both factors and the interaction between them.

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Wu, Z., Autry, A., Bergan, J. et al. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 509, 325–330 (2014). https://doi.org/10.1038/nature13307

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