Cited by 134Neuroendocrine regulation and behaviorMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Organization of neural circuits underlying social behavior: A consideration of the medial amygdala

Open access
Raam, Tara, Hong, Weizhe·2021·Current Opinion in Neurobiology

Abstract

The medial amygdala (MeA) is critical for the expression of a broad range of social behaviors, and is also connected to many other brain regions that mediate those same behaviors. Here, we summarize recent advances toward elucidating mechanisms that enable the MeA to regulate a diversity of social behaviors, and also consider what role the MeA plays within the broader network of regions that orchestrate social sensorimotor transformations. We outline the molecular, anatomical, and electrophysiological features of the MeA that segregate distinct social behaviors, propose experimental strategies to disambiguate sensory representations from behavioral function in the context of a social interaction, and consider to what extent MeA function may overlap with other regions mediating similar behaviors.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.conb.2021.02.008

Cites

17 of 17 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 119

  1. [1]Chen P, Hong W: Neural Circuit Mechanisms of Social Behavior. Neuron 2018, 98: 16– 30. 29621486 PMC6028944
  2. [2]Swanson LW: Cerebral hemisphere regulation of motivated behavior. Brain Res 2000, 886: 113– 164. 11119693
  3. [3]Petrulis A: Structure and Function of the Medial Amygdala. Handb Behav Neurosci 2020, 26: 39– 61.
  4. [4]Newman SW: The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 1999, 877: 242– 257. 10415653
  5. [5]Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB,: Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010, 468: 277– 282. 21068837
  6. [7]Pignatelli M, Beyeler A: Valence coding in amygdala circuits. Curr Opin Behav Sci 2019, 26: 97– 106. 32832584 PMC7440104
  7. [8]Beyeler A, Dabrowska J: Neuronal diversity of the amygdala and the bed nucleus of the stria terminalis. Handb Behav Neurosci 2020, 26: 63– 100. 32792868 PMC7423190
  8. [9]Canteras NS, Simerly RB, Swanson LW: Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 1995, 360: 213– 245. 8522644
  9. [10]Keshavarzi S, Power JM, Albers EH, Sullivan RK, Sah P: Dendritic Organization of Olfactory Inputs to Medial Amygdala Neurons. J Neurosci 2015, 35: 13020– 13028. 26400933 PMC6605442
  10. [11]Li Y, Dulac C: Neural coding of sex-specific social information in the mouse brain. Curr Opin Neurobiol 2018, 53: 120– 130. 30059820
  11. [12]Pro-Sistiaga P, Mohedano-Moriano A, Ubeda-Banon I, Del Mar Arroyo-Jimenez M, Marcos P, Artacho-Perula E, Crespo C, Insausti R, Martinez-Marcos A: Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. J Comp Neurol 2007, 504: 346– 362. 17663431
  12. [14]Keshavarzi S, Sullivan RK, Ianno DJ, Sah P: Functional properties and projections of neurons in the medial amygdala. J Neurosci 2014, 34: 8699– 8715. 24966371 PMC6608208
  13. [15]Pardo-Bellver C, Cadiz-Moretti B, Novejarque A, Martinez-Garcia F, Lanuza E: Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice. Front Neuroanat 2012, 6: 33. 22933993 PMC3423790
  14. [16]Gu G, Cornea A, Simerly RB: Sexual differentiation of projections from the principal nucleus of the bed nuclei of the stria terminalis. J Comp Neurol 2003, 460: 542– 562. 12717713
  15. [17]Akesson TR, Simerly RB, Micevych PE: Estrogen-concentrating hypothalamic and limbic neurons project to the medial preoptic nucleus. Brain Res 1988, 451: 381– 385. 3251599
  16. [18]Canteras NS, Simerly RB, Swanson LW: Organization of projections from the ventromedial nucleus of the hypothalamus: a Phaseolus vulgaris-leucoagglutinin study in the rat. J Comp Neurol 1994, 348: 41– 79. 7814684
  17. [19]Soden ME, Miller SM, Burgeno LM, Phillips PEM, Hnasko TS, Zweifel LS: Genetic Isolation of Hypothalamic Neurons that Regulate Context-Specific Male Social Behavior. Cell Rep 2016, 16: 304– 313. 27346361 PMC4945459
  18. [20]Cadiz-Moretti B, Otero-Garcia M, Martinez-Garcia F, Lanuza E: Afferent projections to the different medial amygdala subdivisions: a retrograde tracing study in the mouse. Brain Struct Funct 2016, 221: 1033– 1065. 25503449
  19. [21]Canteras NS, Simerly RB, Swanson LW: Connections of the posterior nucleus of the amygdala. J Comp Neurol 1992, 324: 143– 179. 1430327
  20. [22]McDonald AJ, Mascagni F: Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1997, 77: 445– 459. 9472403
  21. [23]Turner BH, Gupta KC, Mishkin M: The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta. J Comp Neurol 1978, 177: 381– 396. 412879
  22. [24]Amaral DG, Veazey RB, Cowan WM: Some observations on hypothalamo-amygdaloid connections in the monkey. Brain Res 1982, 252: 13– 27. 6816388
  23. [25]McDonald AJ: Cortical pathways to the mammalian amygdala. Prog Neurobiol 1998, 55: 257– 332. 9643556
  24. [26]Martin LJ, Powers RE, Dellovade TL, Price DL: The bed nucleus-amygdala continuum in human and monkey. J Comp Neurol 1991, 309: 445– 485. 1918444
  25. [27]Hirata T, Li P, Lanuza GM, Cocas LA, Huntsman MM, Corbin JG: Identification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala. Nat Neurosci 2009, 12: 141– 149. 19136974 PMC2747779
  26. [29]Matos HY, Hernandez-Pineda D, Charpentier CM, Rusk A, Corbin JG, Jones KS: Sex Differences in Biophysical Signatures across Molecularly Defined Medial Amygdala Neuronal Subpopulations. eNeuro 2020, 7. PMC7333980 32493755
  27. [30]Soma M, Aizawa H, Ito Y, Maekawa M, Osumi N, Nakahira E, Okamoto H, Tanaka K, Yuasa S: Development of the mouse amygdala as revealed by enhanced green fluorescent protein gene transfer by means of in utero electroporation. J Comp Neurol 2009, 513: 113– 128. 19107806
  28. [31]Zhao T, Szabo N, Ma J, Luo L, Zhou X, Alvarez-Bolado G: Genetic mapping of Foxb1-cell lineage shows migration from caudal diencephalon to telencephalon and lateral hypothalamus. Eur J Neurosci 2008, 28: 1941– 1955. 19046377 PMC2777254
  29. [32]Bupesh M, Legaz I, Abellan A, Medina L: Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol 2011, 519: 1505– 1525. 21452208
  30. [33]Morales L, Castro-Robles B, Abellan A, Desfilis E, Medina L: A novel telencephalon-opto-hypothalamic morphogenetic domain coexpressing Foxg1 and Otp produces most of the glutamatergic neurons of the medial extended amygdala. J Comp Neurol 2021. 33386618
  31. [35]Chen PB, Hu RK, Wu YE, Pan L, Huang S, Micevych PE, Hong W: Sexually Dimorphic Control of Parenting Behavior by the Medial Amygdala. Cell 2019, 176: 1206– 1221 e1218. 30773317 PMC6555485
  32. [36]Xu X, Coats JK, Yang CF, Wang A, Ahmed OM, Alvarado M, Izumi T, Shah NM: Modular genetic control of sexually dimorphic behaviors. Cell 2012, 148: 596– 607. 22304924 PMC3326403
  33. [37]Li Y, Mathis A, Grewe BF, Osterhout JA, Ahanonu B, Schnitzer MJ, Murthy VN, Dulac C: Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice. Cell 2017, 171: 1176– 1190 e1117. 29107332 PMC5731476
  34. [40]Lee W, Dowd HN, Nikain C, Dwortz MF, Yang ED, Curley JP: Effect of relative social rank within a social hierarchy on neural activation in response to familiar or unfamiliar social signals. Sci Rep 2021, 11: 2864. 33536481 PMC7859216
  35. [41]Veening JG, Coolen LM, de Jong TR, Joosten HW, de Boer SF, Koolhaas JM, Olivier B: Do similar neural systems subserve aggressive and sexual behaviour in male rats? Insights from c-Fos and pharmacological studies. Eur J Pharmacol 2005, 526: 226– 239. 16263109
  36. [43]Kemble ED, Blanchard DC, Blanchard RJ, Takushi R: Taming in wild rats following medial amygdaloid lesions. Physiol Behav 1984, 32: 131– 134. 6538976
  37. [44]Takahashi LK, Gladstone CD: Medial amygdaloid lesions and the regulation of sociosexual behavioral patterns across the estrous cycle in female golden hamsters. Behav Neurosci 1988, 102: 268– 275. 3365322
  38. [47]Padilla SL, Qiu J, Soden ME, Sanz E, Nestor CC, Barker FD, Quintana A, Zweifel LS, Ronnekleiv OK, Kelly MJ,: Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state. Nat Neurosci 2016, 19: 734– 741. 27019015 PMC4846501
  39. [48]Nordman JC, Ma X, Gu Q, Potegal M, Li H, Kravitz AV, Li Z: Potentiation of Divergent Medial Amygdala Pathways Drives Experience-Dependent Aggression Escalation. J Neurosci 2020, 40: 4858– 4880. 32424020 PMC7326350
  40. [49]Hashikawa K, Hashikawa Y, Falkner A, Lin D: The neural circuits of mating and fighting in male mice. Curr Opin Neurobiol 2016, 38: 27– 37. 26849838 PMC4921288
  41. [50]Kondo Y: Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiol Behav 1992, 51: 939– 943. 1615054
  42. [51]Rajendren G, Moss RL: The role of the medial nucleus of amygdala in the mating-induced enhancement of lordosis in female rats: the interaction with luteinizing hormone-releasing hormone neuronal system. Brain Res 1993, 617: 81– 86. 8374748
  43. [52]DiBenedictis BT, Ingraham KL, Baum MJ, Cherry JA: Disruption of urinary odor preference and lordosis behavior in female mice given lesions of the medial amygdala. Physiol Behav 2012, 105: 554– 559. 21945865 PMC3279192
  44. [53]Ishii KK, Osakada T, Mori H, Miyasaka N, Yoshihara Y, Miyamichi K, Touhara K: A Labeled-Line Neural Circuit for Pheromone-Mediated Sexual Behaviors in Mice. Neuron 2017, 95: 123– 137 e128. 28648498
  45. [54]Demir E, Li K, Bobrowski-Khoury N, Sanders JI, Beynon RJ, Hurst JL, Kepecs A, Axel R: The pheromone darcin drives a circuit for innate and reinforced behaviours. Nature 2020, 578: 137– 141. 31996852
  46. [55]Fleming AS, Vaccarino F, Luebke C: Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav 1980, 25: 731– 743. 7443835
  47. [56]Numan M, Numan MJ, English JB: Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm Behav 1993, 27: 56– 81. 8440518
  48. [57]Sheehan T, Paul M, Amaral E, Numan MJ, Numan M: Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats. Neuroscience 2001, 106: 341– 356. 11566505
  49. [58]Isogai Y, Wu Z, Love MI, Ahn MH, Bambah-Mukku D, Hua V, Farrell K, Dulac C: Multisensory Logic of Infant-Directed Aggression by Males. Cell 2018, 175: 1827– 1841 e1817. 30550786 PMC6558521
  50. [59]Trouillet AC, Keller M, Weiss J, Leinders-Zufall T, Birnbaumer L, Zufall F, Chamero P: Central role of G protein Galphai2 and Galphai2(+) vomeronasal neurons in balancing territorial and infant-directed aggression of male mice. Proc Natl Acad Sci U S A 2019, 116: 5135– 5143. 30804203 PMC6421405
  51. [60]Tachikawa KS, Yoshihara Y, Kuroda KO: Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J Neurosci 2013, 33: 5120– 5126. 23516278 PMC6705007
  52. [61]Wu Z, Autry AE, Bergan JF, Watabe-Uchida M, Dulac CG: Galanin neurons in the medial preoptic area govern parental behaviour. Nature 2014, 509: 325– 330. 24828191 PMC4105201
  53. [62]Ferguson JN, Aldag JM, Insel TR, Young LJ: Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 2001, 21: 8278– 8285. 11588199 PMC6763861
  54. [63]Gur R, Tendler A, Wagner S: Long-term social recognition memory is mediated by oxytocin-dependent synaptic plasticity in the medial amygdala. Biol Psychiatry 2014, 76: 377– 386. 24787950
  55. [66]Choi GB, Dong HW, Murphy AJ, Valenzuela DM, Yancopoulos GD, Swanson LW, Anderson DJ: Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 2005, 46: 647– 660. 15944132
  56. [67]Miller SM, Marcotulli D, Shen A, Zweifel LS: Divergent medial amygdala projections regulate approach-avoidance conflict behavior. Nat Neurosci 2019, 22: 565– 575. 30804529 PMC6446555
  57. [68]Brothers L, Ring B, Kling A: Response of neurons in the macaque amygdala to complex social stimuli. Behav Brain Res 1990, 41: 199– 213. 2288672
  58. [69]Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG: Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 2007, 97: 1671– 1683. 17093126
  59. [71]Leonard CM, Rolls ET, Wilson FA, Baylis GC: Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 1985, 15: 159– 176. 3994832
  60. [72]Meunier M, Bachevalier J, Murray EA, Malkova L, Mishkin M: Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys. Eur J Neurosci 1999, 11: 4403– 4418. 10594668
  61. [73]Emery NJ, Capitanio JP, Mason WA, Machado CJ, Mendoza SP, Amaral DG: The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta). Behav Neurosci 2001, 115: 515– 544. 11439444
  62. [74]Bickart KC, Hollenbeck MC, Barrett LF, Dickerson BC: Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. J Neurosci 2012, 32: 14729– 14741. 23077058 PMC3569519
  63. [75]Atzil S, Touroutoglou A, Rudy T, Salcedo S, Feldman R, Hooker JM, Dickerson BC, Catana C, Barrett LF: Dopamine in the medial amygdala network mediates human bonding. Proc Natl Acad Sci U S A 2017, 114: 2361– 2366. 28193868 PMC5338494
  64. [76]Bzdok D, Schilbach L, Vogeley K, Schneider K, Laird AR, Langner R, Eickhoff SB: Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy. Brain Struct Funct 2012, 217: 783– 796. 22270812 PMC3445793
  65. [77]Rademacher L, Krach S, Kohls G, Irmak A, Grunder G, Spreckelmeyer KN: Dissociation of neural networks for anticipation and consumption of monetary and social rewards. Neuroimage 2010, 49: 3276– 3285. 19913621
  66. [78]Adolphs R, Baron-Cohen S, Tranel D: Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci 2002, 14: 1264– 1274. 12495531
  67. [79]Becker B, Mihov Y, Scheele D, Kendrick KM, Feinstein JS, Matusch A, Aydin M, Reich H, Urbach H, Oros-Peusquens AM,: Fear processing and social networking in the absence of a functional amygdala. Biol Psychiatry 2012, 72: 70– 77. 22218285
  68. [80]Stowers L, Holy TE, Meister M, Dulac C, Koentges G: Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 2002, 295: 1493– 1500. 11823606
  69. [81]Kimchi T, Xu J, Dulac C: A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 2007, 448: 1009– 1014. 17676034
  70. [82]Harvey CD, Coen P, Tank DW: Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 2012, 484: 62– 68. 22419153 PMC3321074
  71. [83]Driscoll LN, Pettit NL, Minderer M, Chettih SN, Harvey CD: Dynamic Reorganization of Neuronal Activity Patterns in Parietal Cortex. Cell 2017, 170: 986– 999 e916. 28823559 PMC5718200
  72. [84]Alabi OO, Fortunato MP, Fuccillo MV: Behavioral Paradigms to Probe Individual Mouse Differences in Value-Based Decision Making. Front Neurosci 2019, 13: 50. 30792620 PMC6374631
  73. [85]Kingsbury L, Huang S, Wang J, Gu K, Golshani P, Wu YE, Hong W: Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals. Cell 2019, 178: 429– 446 e416. 31230711 PMC6625832
  74. [86]Kingsbury L, Hong W: A Multi-Brain Framework for Social Interaction. Trends Neurosci 2020, 43: 651– 666. 32709376 PMC7484406
  75. [87]Falkner AL, Grosenick L, Davidson TJ, Deisseroth K, Lin D: Hypothalamic control of male aggression-seeking behavior. Nat Neurosci 2016, 19: 596– 604. 26950005 PMC4853470
  76. [88]Golden SA, Heins C, Venniro M, Caprioli D, Zhang M, Epstein DH, Shaham Y: Compulsive Addiction-like Aggressive Behavior in Mice. Biol Psychiatry 2017, 82: 239– 248. 28434654 PMC5532078
  77. [89]Covington HE 3rd, Newman EL, Tran S, Walton L, Hayek W, Leonard MZ, DeBold JF, Miczek KA: The Urge to Fight: Persistent Escalation by Alcohol and Role of NMDA Receptors in Mice. Front Behav Neurosci 2018, 12: 206. 30271332 PMC6146040
  78. [90]Golden SA, Jin M, Shaham Y: Animal Models of (or for) Aggression Reward, Addiction, and Relapse: Behavior and Circuits. J Neurosci 2019, 39: 3996– 4008. 30833504 PMC6529864
  79. [91]Golden SA, Jin M, Heins C, Venniro M, Michaelides M, Shaham Y: Nucleus Accumbens Drd1-Expressing Neurons Control Aggression Self-Administration and Aggression Seeking in Mice. J Neurosci 2019, 39: 2482– 2496. 30655356 PMC6435830
  80. [92]Nordman J, Ma X, Li Z: Traumatic Stress Induces Prolonged Aggression Increase through Synaptic Potentiation in the Medial Amygdala Circuits. eNeuro 2020, 7. PMC7385664 32651265
  81. [93]Nordman J, Li Z: The Dorsal Raphe Regulates the Duration of Attack through the Medial Orbitofrontal Cortex and Medial Amygdala. eNeuro 2020, 7. PMC7665904 33055195
  82. [95]Falkner AL, Dollar P, Perona P, Anderson DJ, Lin D: Decoding ventromedial hypothalamic neural activity during male mouse aggression. J Neurosci 2014, 34: 5971– 5984. 24760856 PMC3996217
  83. [96]Remedios R, Kennedy A, Zelikowsky M, Grewe BF, Schnitzer MJ, Anderson DJ: Social behaviour shapes hypothalamic neural ensemble representations of conspecific sex. Nature 2017, 550: 388– 392. 29052632 PMC5674977
  84. [97]Kingsbury L, Huang S, Raam T, Ye LS, Wei D, Hu RK, Ye L, Hong W: Cortical Representations of Conspecific Sex Shape Social Behavior. Neuron 2020, 107: 941– 953 e947. 32663438 PMC7486272
  85. [98]Levy DR, Tamir T, Kaufman M, Parabucki A, Weissbrod A, Schneidman E, Yizhar O: Dynamics of social representation in the mouse prefrontal cortex. Nat Neurosci 2019, 22: 2013– 2022. 31768051
  86. [99]Zhou T, Zhu H, Fan Z, Wang F, Chen Y, Liang H, Yang Z, Zhang L, Lin L, Zhan Y,: History of winning remodels thalamo-PFC circuit to reinforce social dominance. Science 2017, 357: 162– 168. 28706064
  87. [101]Raam T: Oxytocin-Sensitive Neurons in Prefrontal Cortex Gate Social Recognition Memory. J Neurosci 2020, 40: 1194– 1196. 32024768 PMC7002152
  88. [103]Rao RP, von Heimendahl M, Bahr V, Brecht M: Neuronal Responses to Conspecifics in the Ventral CA1. Cell Rep 2019, 27: 3460– 3472 e3463. 31216468
  89. [104]Leroy F, Park J, Asok A, Brann DH, Meira T, Boyle LM, Buss EW, Kandel ER, Siegelbaum SA: A circuit from hippocampal CA2 to lateral septum disinhibits social aggression. Nature 2018, 564: 213– 218. 30518859 PMC6364572
  90. [105]Yamaguchi T, Wei D, Song SC, Lim B, Tritsch NX, Lin D: Posterior amygdala regulates sexual and aggressive behaviors in male mice. Nat Neurosci 2020, 23: 1111– 1124. 32719562 PMC7483354
  91. [106]Stagkourakis S, Spigolon G, Liu G, Anderson DJ: Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP. Proc Natl Acad Sci U S A 2020, 117: 25789– 25799. 32973099 PMC7568289
  92. [107]Zha X, Wang L, Jiao ZL, Yang RR, Xu C, Xu XH: VMHvl-Projecting Vglut1+ Neurons in the Posterior Amygdala Gate Territorial Aggression. Cell Rep 2020, 31: 107517. 32320666
  93. [108]Bayless DW, Yang T, Mason MM, Susanto AAT, Lobdell A, Shah NM: Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males. Cell 2019, 176: 1190– 1205 e1120. 30712868 PMC6453703
  94. [109]Zelikowsky M, Hui M, Karigo T, Choe A, Yang B, Blanco MR, Beadle K, Gradinaru V, Deverman BE, Anderson DJ: The Neuropeptide Tac2 Controls a Distributed Brain State Induced by Chronic Social Isolation Stress. Cell 2018, 173: 1265– 1279 e1219. 29775595 PMC5967263
  95. [110]Falkner AL, Wei D, Song A, Watsek LW, Chen I, Chen P, Feng JE, Lin D: Hierarchical Representations of Aggression in a Hypothalamic-Midbrain Circuit. Neuron 2020, 106: 637– 648 e636. 32164875 PMC7571490
  96. [111]Fang YY, Yamaguchi T, Song SC, Tritsch NX, Lin D: A Hypothalamic Midbrain Pathway Essential for Driving Maternal Behaviors. Neuron 2018, 98: 192– 207 e110. 29621487 PMC5890946
  97. [112]Kohl J, Babayan BM, Rubinstein ND, Autry AE, Marin-Rodriguez B, Kapoor V, Miyamishi K, Zweifel LS, Luo L, Uchida N,: Functional circuit architecture underlying parental behaviour. Nature 2018, 556: 326– 331. 29643503 PMC5908752
  98. [113]Li XY, Han Y, Zhang W, Wang SR, Wei YC, Li SS, Lin JK, Yan JJ, Chen AX, Zhang X,: AGRP Neurons Project to the Medial Preoptic Area and Modulate Maternal Nest-Building. J Neurosci 2019, 39: 456– 471. 30459220 PMC6335756
  99. [114]Stagkourakis S, Smiley KO, Williams P, Kakadellis S, Ziegler K, Bakker J, Brown RSE, Harkany T, Grattan DR, Broberger C: A Neuro-hormonal Circuit for Paternal Behavior Controlled by a Hypothalamic Network Oscillation. Cell 2020, 182: 960– 975 e915. 32763155 PMC7445434
  100. [115]Kohl J: Parenting - a paradigm for investigating the neural circuit basis of behavior. Curr Opin Neurobiol 2020, 60: 84– 91. 31830690 PMC7005672
  101. [116]Wei YC, Wang SR, Jiao ZL, Zhang W, Lin JK, Li XY, Li SS, Zhang X, Xu XH: Medial preoptic area in mice is capable of mediating sexually dimorphic behaviors regardless of gender. Nat Commun 2018, 9: 279. 29348568 PMC5773506
  102. [117]Marlin BJ, Mitre M, D’Amour JA, Chao MV, Froemke RC: Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 2015, 520: 499– 504. 25874674 PMC4409554
  103. [118]Schiavo JK, Valtcheva S, Bair-Marshall CJ, Song SC, Martin KA, Froemke RC: Innate and plastic mechanisms for maternal behaviour in auditory cortex. Nature 2020. PMC7677212 33029014
  104. [119]Tasaka GI, Feigin L, Maor I, Groysman M, DeNardo LA, Schiavo JK, Froemke RC, Luo L, Mizrahi A: The Temporal Association Cortex Plays a Key Role in Auditory-Driven Maternal Plasticity. Neuron 2020, 107: 566– 579 e567. 32473095 PMC8725613
  105. [121]Oliva A, Fernandez-Ruiz A, Leroy F, Siegelbaum SA: Hippocampal CA2 sharp-wave ripples reactivate and promote social memory. Nature 2020. PMC7666067 32968277
  106. [122]Okuyama T, Kitamura T, Roy DS, Itohara S, Tonegawa S: Ventral CA1 neurons store social memory. Science 2016, 353: 1536– 1541. 27708103 PMC5493325
  107. [123]Meira T, Leroy F, Buss EW, Oliva A, Park J, Siegelbaum SA: A hippocampal circuit linking dorsal CA2 to ventral CA1 critical for social memory dynamics. Nat Commun 2018, 9: 4163. 30301899 PMC6178349
  108. [124]Deng X, Gu L, Sui N, Guo J, Liang J: Parvalbumin interneuron in the ventral hippocampus functions as a discriminator in social memory. Proc Natl Acad Sci U S A 2019, 116: 16583– 16592. 31358646 PMC6697894
  109. [125]Tan Y, Singhal SM, Harden SW, Cahill KM, Nguyen DM, Colon-Perez LM, Sahagian TJ, Thinschmidt JS, de Kloet AD, Febo M,: Oxytocin Receptors Are Expressed by Glutamatergic Prefrontal Cortical Neurons That Selectively Modulate Social Recognition. J Neurosci 2019, 39: 3249– 3263. 30804095 PMC6788819
  110. [127]Pereira TD, Tabris N, Li J, Ravindranath S, Papadoyannis ES, Wang ZY, Turner DM, McKenzie-Smith G, Kocher SD, Falkner AL,: SLEAP: Multi-animal pose tracking. bioRxiv 2020:2020.2008.2031.276246.
  111. [128]Steinmetz NA, Zatka-Haas P, Carandini M, Harris KD: Distributed coding of choice, action and engagement across the mouse brain. Nature 2019, 576: 266– 273. 31776518 PMC6913580
  112. [129]Stringer C, Pachitariu M, Steinmetz N, Reddy CB, Carandini M, Harris KD: Spontaneous behaviors drive multidimensional, brainwide activity. Science 2019, 364: 255. 31000656 PMC6525101
  113. [130]Kim CK, Yang SJ, Pichamoorthy N, Young NP, Kauvar I, Jennings JH, Lerner TN, Berndt A, Lee SY, Ramakrishnan C,: Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain. Nat Methods 2016, 13: 325– 328. 26878381 PMC5717315
  114. [131]Sych Y, Chernysheva M, Sumanovski LT, Helmchen F: High-density multi-fiber photometry for studying large-scale brain circuit dynamics. Nat Methods 2019, 16: 553– 560. 31086339
  115. [132]Luo TZ, Bondy AG, Gupta D, Elliott VA, Kopec CD, Brody CD: An approach for long-term, multi-probe Neuropixels recordings in unrestrained rats. Elife 2020, 9. PMC7721443 33089778
  116. [133]Mathis A, Mamidanna P, Cury KM, Abe T, Murthy VN, Mathis MW, Bethge M: DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat Neurosci 2018, 21: 1281– 1289. 30127430
  117. [134]Nilsson SR, Goodwin NL, Choong JJ, Hwang S, Wright HR, Norville ZC, Tong X, Lin D, Bentzley BS, Eshel N,: Simple Behavioral Analysis (SimBA) – an open source toolkit for computer classification of complex social behaviors in experimental animals. bioRxiv 2020:2020.2004.2019.049452.
  118. [135]Hong W, Kennedy A, Burgos-Artizzu XP, Zelikowsky M, Navonne SG, Perona P, Anderson DJ: Automated measurement of mouse social behaviors using depth sensing, video tracking, and machine learning. Proc Natl Acad Sci U S A 2015, 112: E5351– 5360. 26354123 PMC4586844
  119. [136]Wiltschko AB, Johnson MJ, Iurilli G, Peterson RE, Katon JM, Pashkovski SL, Abraira VE, Adams RP, Datta SR: Mapping Sub-Second Structure in Mouse Behavior. Neuron 2015, 88: 1121– 1135. 26687221 PMC4708087

Cited by

Sorted by citations

Authors
Raam, T., & Hong, W.
Affiliations
University of California, Los Angeles (US)
Corresponding author
Hong, Weizhe
Venue
Current Opinion in Neurobiology
Publisher
Elsevier BV
Published
2021-06
Volume
68
Pages
124-136
ISSN
0959-4388 (ISSN-L)
OpenAlex
W3159665035
Cited by
134
References
17
Citations by year
2026: 20 · 2025: 33 · 2024: 29 · 2023: 27 · 2022: 20 · 2021: 5
FWCI
3.18
Type
journal article
Language
en
Open access
Locations
  • Current Opinion in Neurobiology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institutes of Health (T32-NS048004, RF1-DA048811, R01-NS113124, F32-MH123049)
  • Esther A and Joseph Klingenstein Fund Inc
  • Searle Scholars Program
  • Edward Mallinckrodt Jr Foundation
  • W M Keck Foundation
  • Bert L and N Kuggie Vallee Foundation
  • McKnight Foundation
  • McKnight Endowment Fund for Neuroscience
  • David and Lucile Packard Foundation
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
medial amygdala, social behavior, neural circuits, sensory representation, social interaction, electrophysiology, molecular mechanisms, structural connectivity
MeSH terms
Amygdala, Social Behavior, Electrophysiological Phenomena

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review