Parenting — a paradigm for investigating the neural circuit basis of behavior

Highlights • Molecularly defined nodes have been identified in parental circuits.• A functional circuit logic of parental behavior is emerging.• Parenting relies on largely similar circuitry in males and females.• Infant-directed aggression is controlled by dedicated circuits.

[1]  Y. Yoshihara,et al.  Behavioral Transition from Attack to Parenting in Male Mice: A Crucial Role of the Vomeronasal System , 2013, The Journal of Neuroscience.

[2]  Jacob M. Graving,et al.  DeepPoseKit, a software toolkit for fast and robust animal pose estimation using deep learning , 2019, bioRxiv.

[3]  Guo-Cheng Yuan,et al.  Transcriptome-scale super-resolved imaging in tissues by RNA seqFISH+ , 2019, Nature.

[4]  Sergey L. Gratiy,et al.  Fully integrated silicon probes for high-density recording of neural activity , 2017, Nature.

[5]  Kazunari Miyamichi,et al.  Sexual rejection via a vomeronasal receptor-triggered limbic circuit , 2018, Nature Communications.

[6]  M. Love,et al.  Multisensory Logic of Infant-Directed Aggression by Males , 2018, Cell.

[7]  Kevin M. Cury,et al.  DeepLabCut: markerless pose estimation of user-defined body parts with deep learning , 2018, Nature Neuroscience.

[8]  William E. Allen,et al.  Three-dimensional intact-tissue sequencing of single-cell transcriptional states , 2018, Science.

[9]  D. Lukas,et al.  The evolution of infanticide by males in mammalian societies , 2014, Science.

[10]  T. Sheehan,et al.  Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats , 2001, Neuroscience.

[11]  Wei L. Shen,et al.  AGRP Neurons Project to the Medial Preoptic Area and Modulate Maternal Nest-Building , 2018, The Journal of Neuroscience.

[12]  Taiju Amano,et al.  Development-dependent behavioral change toward pups and synaptic transmission in the rhomboid nucleus of the bed nucleus of the stria terminalis , 2017, Behavioural Brain Research.

[13]  Yuchio Yanagawa,et al.  Molecular interrogation of hypothalamic organization reveals distinct dopamine neuronal subtypes , 2016, Nature Neuroscience.

[14]  William E. Allen,et al.  Thirst regulates motivated behavior through modulation of brainwide neural population dynamics , 2019, Science.

[15]  J. Labov Factors influencing infanticidal behavior in wild male house mice (Mus musculus) , 1980, Behavioral Ecology and Sociobiology.

[16]  Minmin Luo,et al.  A Neural Circuit Driving Maternal Behaviors , 2018, Neuron.

[17]  Ofer Yizhar,et al.  A sexually dimorphic hypothalamic circuit controls maternal care and oxytocin secretion , 2015, Nature.

[18]  C. Dulac,et al.  Genetic analysis of brain circuits underlying pheromone signaling. , 2006, Annual review of genetics.

[19]  Frank Buchholz,et al.  Dre recombinase, like Cre, is a highly efficient site-specific recombinase in E. coli, mammalian cells and mice , 2009, Disease Models & Mechanisms.

[20]  Ana González-Rueda,et al.  Life-Long Genetic and Functional Access to Neural Circuits Using Self-Inactivating Rabies Virus , 2017, Cell.

[21]  Nimrod D. Rubinstein,et al.  Perifornical Area Urocortin-3 Neurons Promote Infant-directed Neglect and Aggression , 2019 .

[22]  Fei Zhao,et al.  Anterograde monosynaptic transneuronal tracers derived from herpes simplex virus 1 strain H129 , 2017, Molecular Neurodegeneration.

[23]  F. S. Saal Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice , 1985, Physiology & Behavior.

[24]  Yun-Hee Choi,et al.  Revisiting the Ventral Medial Nucleus of the Hypothalamus: The Roles of SF-1 Neurons in Energy Homeostasis , 2013, Front. Neurosci..

[25]  Julie Harris,et al.  Connectional architecture of a mouse hypothalamic circuit node controlling social behavior , 2018, Proceedings of the National Academy of Sciences.

[26]  Richard Bonneau,et al.  High-density spatial transcriptomics arrays for in situ tissue profiling , 2019, bioRxiv.

[27]  L. Looger,et al.  A Designer AAV Variant Permits Efficient Retrograde Access to Projection Neurons , 2016, Neuron.

[28]  Kenneth D. Harris,et al.  High-dimensional geometry of population responses in visual cortex , 2019, Nat..

[29]  M. Andermann,et al.  Toward a Wiring Diagram Understanding of Appetite Control , 2017, Neuron.

[30]  Evan Z. Macosko,et al.  Slide-seq: A scalable technology for measuring genome-wide expression at high spatial resolution , 2019, Science.

[31]  Benjamin F. Grewe,et al.  Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice , 2017, Cell.

[32]  Cheuk Y. Tang,et al.  Mapping of Brain Activity by Automated Volume Analysis of Immediate Early Genes , 2016, Cell.

[33]  F. V. vom Saal Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. , 1985, Physiology & behavior.

[34]  F. Buchholz,et al.  A single reporter mouse line for Vika, Flp, Dre, and Cre-recombination , 2018, Scientific Reports.

[35]  Wen Zhang,et al.  Medial preoptic area in mice is capable of mediating sexually dimorphic behaviors regardless of gender , 2018, Nature Communications.

[36]  C. Dulac,et al.  Neural control of maternal and paternal behaviors , 2014, Science.

[37]  V. Gradinaru,et al.  Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems , 2017, Nature Neuroscience.

[38]  Attila Losonczy,et al.  Rabies Virus CVS-N2cΔG Strain Enhances Retrograde Synaptic Transfer and Neuronal Viability , 2016, Neuron.

[39]  M. Yoshihara,et al.  ‘Necessary and sufficient’ in biology is not necessarily necessary – confusions and erroneous conclusions resulting from misapplied logic in the field of biology, especially neuroscience , 2018, Journal of neurogenetics.

[40]  F. Zufall,et al.  Central role of G protein Gαi2 and Gαi2+ vomeronasal neurons in balancing territorial and infant-directed aggression of male mice , 2019, Proceedings of the National Academy of Sciences.

[41]  F. Esposti,et al.  Targeting neuronal and glial cell types with synthetic promoter AAVs in mice, non-human primates and humans , 2018, Nature Neuroscience.

[42]  Gianluca Esposito,et al.  Distinct preoptic‐BST nuclei dissociate paternal and infanticidal behavior in mice , 2015, The EMBO journal.

[43]  Nimrod D. Rubinstein,et al.  Functional circuit architecture underlying parental behaviour , 2018, Nature.

[44]  A. Bartke,et al.  Food deprivation induces conspecific pup‐killing in mice , 1978 .

[45]  Garreck H. Lenz,et al.  Prospective, brain-wide labeling of neuronal subclasses with enhancer-driven AAVs , 2019, bioRxiv.

[46]  M. Numan,et al.  Medial preoptic area and maternal behavior in the female rat. , 1974, Journal of comparative and physiological psychology.

[47]  Nimrod D. Rubinstein,et al.  Molecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region , 2018, Science.

[48]  Georg B. Keller,et al.  Expression of c-Fos and Arc in hippocampal region CA1 marks neurons that exhibit learning-related activity changes , 2019, bioRxiv.

[49]  Arjun Bharioke,et al.  Targeting neuronal and glial cell types with synthetic promoter AAVs in mice, non-human primates, and humans , 2018, bioRxiv.

[50]  Mitsuko Watabe-Uchida,et al.  Galanin neurons in the medial preoptic area govern parental behavior , 2014, Nature.

[51]  Ian R. Wickersham,et al.  Nontoxic, double-deletion-mutant rabies viral vectors for retrograde targeting of projection neurons , 2018, Nature Neuroscience.

[52]  T. Hökfelt,et al.  Unified Classification of Molecular, Network, and Endocrine Features of Hypothalamic Neurons. , 2019, Annual review of neuroscience.

[53]  S. Parmigiani,et al.  Infanticide and Parental Care , 1994 .

[54]  T. Kimchi,et al.  Sexual Dimorphism of Parental Care: From Genes to Behavior. , 2017, Annual review of neuroscience.

[55]  H. Gainer,et al.  Cell-Type Specific Oxytocin Gene Expression from AAV Delivered Promoter Deletion Constructs into the Rat Supraoptic Nucleus in vivo , 2012, PloS one.

[56]  S. Hrdy,et al.  Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females , 1979 .

[57]  J. Betley,et al.  Parallel, Redundant Circuit Organization for Homeostatic Control of Feeding Behavior , 2013, Cell.

[58]  Shaoqun Zeng,et al.  Brain-wide single neuron reconstruction reveals morphological diversity in molecularly defined striatal, thalamic, cortical and claustral neuron types , 2019, bioRxiv.

[59]  Nathan C. Klapoetke,et al.  Transgenic Mice for Intersectional Targeting of Neural Sensors and Effectors with High Specificity and Performance , 2015, Neuron.

[60]  Justus M. Kebschull,et al.  High-Throughput Mapping of Single-Neuron Projections by Sequencing of Barcoded RNA , 2016, Neuron.

[61]  D. Lukas,et al.  The evolution of infanticide by females in mammals , 2018, bioRxiv.

[62]  Charles R. Gerfen,et al.  Reconstruction of 1,000 Projection Neurons Reveals New Cell Types and Organization of Long-Range Connectivity in the Mouse Brain , 2019, Cell.

[63]  Nicholas A. Steinmetz,et al.  Spontaneous behaviors drive multidimensional, brainwide activity , 2019, Science.

[64]  David J. Anderson,et al.  Scalable Control of Mounting and Attack by ESR1+ Neurons in the Ventromedial Hypothalamus , 2014, Nature.

[65]  Dayu Lin,et al.  A Hypothalamic Midbrain Pathway Essential for Driving Maternal Behaviors , 2018, Neuron.

[66]  B. Harris,et al.  Effects of repeated pup exposure on behavioral, neural, and adrenocortical responses to pups in male California mice (Peromyscus californicus) , 2017, Hormones and Behavior.

[67]  David J. Anderson,et al.  Automated measurement of mouse social behaviors using depth sensing, video tracking, and machine learning , 2015, Proceedings of the National Academy of Sciences.

[68]  R. Kageyama,et al.  In vivo evaluation of PhiC31 recombinase activity in transgenic mice , 2012, Neuroscience Research.

[69]  Annegret L. Falkner,et al.  The neural circuits of mating and fighting in male mice , 2016, Current Opinion in Neurobiology.

[70]  Patrik L. Ståhl,et al.  Visualization and analysis of gene expression in tissue sections by spatial transcriptomics , 2016, Science.

[71]  J. Rubenstein,et al.  An estrogen-responsive module in the ventromedial hypothalamus selectively drives sex-specific activity in females. , 2015, Cell reports.

[72]  Yoshihiro Yoshihara,et al.  A Labeled-Line Neural Circuit for Pheromone-Mediated Sexual Behaviors in Mice , 2017, Neuron.

[73]  M. Numan,et al.  Excitotoxic Amino Acid Injections into the Medial Amygdala Facilitate Maternal Behavior in Virgin Female Rats , 1993, Hormones and Behavior.

[74]  J. Power,et al.  Dendritic Organization of Olfactory Inputs to Medial Amygdala Neurons , 2015, The Journal of Neuroscience.

[75]  T. Insel,et al.  The Neurobiology of Parental Behavior , 2003, Hormones, Brain, and Behavior.