CoChat
Sign Up
Cited by 71Neuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Coordination of social behaviors by the bed nucleus of the stria terminalis

Open access
Flanigan, Meghan E., Kash, Thomas L.·2022·European Journal of Neuroscience
DOI 10.1111/ejn.14991PMC PMC9906816
Open this paper in CoChat — free account

Abstract

The bed nucleus of the stria terminalis (BNST) is a sexually dimorphic, neuropeptide‐rich node of the extended amygdala that has been implicated in responses to stress, drugs of abuse, and natural rewards. Its function is dysregulated in neuropsychiatric disorders that are characterized by stress‐ or drug‐induced alterations in mood, arousal, motivation, and social behavior. However, compared to the BNST’s role in mood, arousal, and motivation, its role in social behavior has remained relatively understudied. Moreover, the precise cell types and circuits underlying the BNST’s role in social behavior have only recently begun to be explored using modern neuroscience techniques. Here, we systematically review the existing literature investigating the neurobiological substrates within the BNST that contribute to the coordination of various sex‐dependent and sex‐independent social behavioral repertoires, focusing largely on pharmacological and circuit‐based behavioral studies in rodents. We suggest that the BNST coordinates social behavior by promoting appropriate assessment of social contexts to select relevant behavioral outputs and that disruption of socially relevant BNST systems by stress and drugs of abuse may be an important factor in the development of social dysfunction in neuropsychiatric disorders.

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 · 10.1111/ejn.14991

Cites

27 of 27 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?

  • Male gonadal hormones act during puberty to reduce negative valence assessments of novel social contexts, an important function of the BNST.

    “These data suggest that male gonadal hormones act during puberty to reduce negative valence assessments of novel social contexts, an important function of the BNST (74, 75).”

    From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [74]

    The Introduction (page not provided) proposes that the BNST evaluates social targets and the context of an interaction, including potential threats. The section on aggressive social behaviors describes testosterone-responsive BNST neurons reacting to an unfamiliar male, but does not say that male gonadal hormones act during puberty to reduce negative assessments of novel social contexts. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

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: 122

  1. Aleyasin H, Flanigan ME, Golden SA, Takahashi A, Menard C, Pfau ML, Multer J, Pina J, McCabe KA, Bhatti N, Hodes GE, Heshmati M, Neve RL, Nestler EJ, Heller EA & Russo SJ (2018) Cell-Type-Specific Role of ΔFosB in Nucleus Accumbens In Modulating Intermale Aggression. J Neurosci, 38, 5913– 5924. 29891732 PMC6021989
  2. Anpilov S, Shemesh Y, Eren N, Harony-Nicolas H, Benjamin A, Dine J, Oliveira VEM, Forkosh O, Karamihalev S, Hüttl RE, Feldman N, Berger R, Dagan A, Chen G, Neumann ID, Wagner S, Yizhar O & Chen A (2020) Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors. Neuron. PMC7447984 32544386
  3. Avery SN, Clauss JA & Blackford JU (2016) The Human BNST: Functional Role in Anxiety and Addiction. Neuropsychopharmacology, 41, 126– 141. 26105138 PMC4677124
  4. Bamshad M, Cooper TT, Karom M & Albers HE (1996) Glutamate and vasopressin interact to control scent marking in Syrian hamsters (Mesocricetus auratus). Brain Res, 731, 213– 216. 8883873
  5. Barnea-Ygael N, Gal R & Zangen A (2016) Chronic cocaine administration induces long-term impairment in the drive to obtain natural reinforcers in high- but not low-demanding tasks. Addiction biology, 21, 294– 303. 25393705
  6. Bartal IB-A, Decety J & Mason P (2011) Empathy and pro-social behavior in rats. Science, 334, 1427– 1430. 22158823 PMC3760221
  7. Bayless DW, Yang T, Mason MM, Susanto AAT, Lobdell A & Shah NM (2019) Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males. Cell, 176, 1190– 1205.e1120. 30712868 PMC6453703
  8. Blanchard DC, Fukunaga-Stinson C, Takahashi LK, Flannelly KJ & Blanchard RJ (1984) Dominance and aggression in social groups of male and female rats. Behav Processes, 9, 31– 48. 24923827
  9. Blanco-Gandía MC, Mateos-García A, García-Pardo MP, Montagud-Romero S, Rodríguez-Arias M, Miñarro J & Aguilar MA (2015) Effect of drugs of abuse on social behaviour: a review of animal models. Behav Pharmacol, 26, 541– 570. 26221831
  10. Bosch O, Pförtsch J, Beiderbeck D, Landgraf R & Neumann I (2010) Maternal behaviour is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. Journal of neuroendocrinology, 22, 420– 429. 20163514
  11. Bosch OJ (2011) Maternal nurturing is dependent on her innate anxiety: the behavioral roles of brain oxytocin and vasopressin. Horm Behav, 59, 202– 212. 21094649
  12. Brayley KN & Albert DJ (1977) Suppression of VMH-lesion-induced reactivity and aggressiveness in the rat by stimulation of lateral septum, but not medial septum or cingulate cortex. J Comp Physiol Psych, 91, 290– 299. 558231
  13. Brinkmann L, Buff C, Feldker K, Neumeister P, Heitmann CY, Hofmann D, Bruchmann M, Herrmann MJ & Straube T (2018) Inter-individual differences in trait anxiety shape the functional connectivity between the bed nucleus of the stria terminalis and the amygdala during brief threat processing. Neuroimage, 166, 110– 116. 29107120
  14. Buff C, Brinkmann L, Bruchmann M, Becker MPI, Tupak S, Herrmann MJ & Straube T (2017) Activity alterations in the bed nucleus of the stria terminalis and amygdala during threat anticipation in generalized anxiety disorder. Soc Cogn Affect Neurosci, 12, 1766– 1774. 28981839 PMC5714227
  15. Calcagnoli F, de Boer SF, Beiderbeck DI, Althaus M, Koolhaas JM & Neumann ID (2014) Local oxytocin expression and oxytocin receptor binding in the male rat brain is associated with aggressiveness. Behav Brain Res, 261, 315– 322. 24406721
  16. Campi KL, Jameson CE & Trainor BC (2013) Sexual Dimorphism in the Brain of the Monogamous California Mouse (Peromyscus californicus). Brain Behav Evol, 81, 236– 249. 23881046 PMC3915401
  17. Canteras NS, Simerly RB & Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol, 360, 213– 245. 8522644
  18. Castellano F, Bartoli F, Crocamo C, Gamba G, Tremolada M, Santambrogio J, Clerici M & Carrà G (2015) Facial emotion recognition in alcohol and substance use disorders: A meta-analysis. Neurosci Biobehav Rev, 59, 147– 154. 26546735
  19. Champagne F, Diorio J, Sharma S & Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A, 98, 12736– 12741. 11606726 PMC60123
  20. Claro F, Segovia S, Guilamón A & Del Abril A (1995) Lesions in the medial posterior region of the BST impair sexual behavior in sexually experienced and inexperienced male rats. Brain research bulletin, 36, 1– 10. 7882041
  21. Clauss JA, Avery SN, Benningfield MM & Blackford JU (2019) Social anxiety is associated with BNST response to unpredictability. Depression and Anxiety, 36, 666– 675. 30953446 PMC6679811
  22. Consiglio AR, Borsoi A, Pereira GA & Lucion AB (2005) Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol Behav, 85, 354– 362. 15935410
  23. Cooper MA & Huhman KL (2010) Blocking corticotropin-releasing factor-2 receptors, but not corticotropin-releasing factor-1 receptors or glucocorticoid feedback, disrupts the development of conditioned defeat. Physiol Behav, 101, 527– 532. 20705077 PMC2949480
  24. Davis BJ, Macrides F, Youngs WM, Schneider SP & Rosene DL (1978) Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster. Brain Research Bulletin, 3, 59– 72. 75756
  25. Davis ES & Marler CA (2004) c-fos Changes following an aggressive encounter in female California mice: a synthesis of behavior, hormone changes and neural activity. Neuroscience, 127, 611– 624. 15283961
  26. Dolen G, Darvishzadeh A, Huang KW & Malenka RC (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature, 501, 179– 184. 24025838 PMC4091761
  27. Dong HW & Swanson LW (2004a) Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J Comp Neurol, 468, 277– 298. 14648685
  28. Dong HW & Swanson LW (2004b) Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J Comp Neurol, 471, 396– 433. 15022261
  29. Dong HW & Swanson LW (2006a) Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol, 494, 142– 178. 16304685 PMC2563961
  30. Dong HW & Swanson LW (2006b) Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J Comp Neurol, 494, 75– 107. 16304681 PMC2707828
  31. Dumais KM, Alonso AG, Immormino MA, Bredewold R & Veenema AH (2016) Involvement of the oxytocin system in the bed nucleus of the stria terminalis in the sex-specific regulation of social recognition. Psychoneuroendocrinology, 64, 79– 88. 26630388 PMC4698213
  32. Duque-Wilckens N, Steinman MQ, Laredo SA, Hao R, Perkeybile AM, Bales KL & Trainor BC (2016) Inhibition of vasopressin V1a receptors in the medioventral bed nucleus of the stria terminalis has sex- and context-specific anxiogenic effects. Neuropharmacology, 110, 59– 68. 27452721 PMC5028294
  33. Emmons R, Sadok T, Rovero NG, Belnap MA, Henderson HJM, Quan AJ, Del Toro NJ & Halladay LR (2020) Chemogenetic manipulation of the bed nucleus of the stria terminalis counteracts social behavioral deficits induced by early life stress in C57BL/6J mice. J Neurosci Res. 32476178
  34. Falkner AL, Grosenick L, Davidson TJ, Deisseroth K & Lin D (2016) Hypothalamic control of male aggression-seeking behavior. Nat Neurosci, 19, 596– 604. 26950005 PMC4853470
  35. Ferrero DM, Moeller LM, Osakada T, Horio N, Li Q, Roy DS, Cichy A, Spehr M, Touhara K & Liberles SD (2013) A juvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system. Nature, 502, 368– 371. 24089208 PMC3800207
  36. Ferris CF, Stolberg T, Kulkarni P, Murugavel M, Blanchard R, Blanchard DC, Febo M, Brevard M & Simon NG (2008) Imaging the neural circuitry and chemical control of aggressive motivation. BMC Neurosci, 9, 111. 19014547 PMC2601047
  37. Figel B, Brinkmann L, Buff C, Heitmann CY, Hofmann D, Bruchmann M, Becker MPI, Herrmann MJ & Straube T (2019) Phasic amygdala and BNST activation during the anticipation of temporally unpredictable social observation in social anxiety disorder patients. Neuroimage Clin, 22, 101735. 30878610 PMC6423472
  38. Fink G, Sumner BE, Rosie R, Grace O & Quinn JP (1996) Estrogen control of central neurotransmission: effect on mood, mental state, and memory. Cell Mol Neurobiol, 16, 325– 344. 8818400 PMC11563142
  39. Flanigan ME, Aleyasin H, Li L, Burnett CJ, Chan KL, LeClair KB, Lucas EK, Matikainen-Ankney B, Durand-de Cuttoli R, Takahashi A, Menard C, Pfau ML, Golden SA, Bouchard S, Calipari ES, Nestler EJ, DiLeone RJ, Yamanaka A, Huntley GW, Clem RL & Russo SJ (2020) Orexin signaling in GABAergic lateral habenula neurons modulates aggressive behavior in male mice. Nat Neurosci, 23, 638– 650. 32284606 PMC7195257
  40. Flannelly KJ, Blanchard RJ, Muraoka MY & Flannelly L (1982) Copulation increases offensive attack in male rats. Physiol Behav, 29, 381– 385. 6890693
  41. Fuxjager MJ, Forbes-Lorman RM, Coss DJ, Auger CJ, Auger AP & Marler CA (2010) Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc Natl Acad Sci U S A, 107, 12393– 12398. 20616093 PMC2901436
  42. Golden SA, Heins C, Venniro M, Caprioli D, Zhang M, Epstein DH & Shaham Y (2017) Compulsive Addiction-like Aggressive Behavior in Mice. Biol Psychiatry, 82, 239– 248. 28434654 PMC5532078
  43. Golden SA, Heshmati M, Flanigan M, Christoffel DJ, Guise K, Pfau ML, Aleyasin H, Menard C, Zhang H, Hodes GE, Bregman D, Khibnik L, Tai J, Rebusi N, Krawitz B, Chaudhury D, Walsh JJ, Han MH, Shapiro ML & Russo SJ (2016) Basal forebrain projections to the lateral habenula modulate aggression reward. Nature, 534, 688– 692. 27357796 PMC4930107
  44. Golden SA, Jin M, Heins C, Venniro M, Michaelides M & Shaham Y (2019) Nucleus Accumbens Drd1-Expressing Neurons Control Aggression Self-Administration and Aggression Seeking in Mice. J Neurosci, 39, 2482– 2496. 30655356 PMC6435830
  45. Greenberg G, Laman-Maharg A, Campi K, Voigt H, Orr V, Schaal L & Trainor B (2014a) Sex differences in stress-induced social withdrawal: role of brain derived neurotrophic factor in the bed nucleus of the stria terminalis. Frontiers in Behavioral Neuroscience, 7. PMC3885825 24409132
  46. Greenberg GD, Howerton CL & Trainor BC (2014b) Fighting in the home cage: Agonistic encounters and effects on neurobiological markers within the social decision-making network of house mice (Mus musculus). Neurosci Lett, 566, 151– 155. 24602985 PMC4019314
  47. Guarraci FA & Bolton JL (2014) “Sexy stimulants”: The interaction between psychomotor stimulants and sexual behavior in the female brain. Pharmacology Biochemistry and Behavior, 121, 53– 61. 24269964
  48. Guarraci FA & Clark AS (2003) Amphetamine modulation of paced mating behavior. Pharmacology, biochemistry, and behavior, 76, 505– 515. 14643850
  49. Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE, Adhikari A, Lammel S, Mirzabekov JJ, Airan RD, Zalocusky KA, Tye KM, Anikeeva P, Malenka RC & Deisseroth K (2014) Natural neural projection dynamics underlying social behavior. Cell, 157, 1535– 1551. 24949967 PMC4123133
  50. Haller J, Tóth M, Halasz J & De Boer SF (2006) Patterns of violent aggression-induced brain c-fos expression in male mice selected for aggressiveness. Physiol Behav, 88, 173– 182. 16687160
  51. Hamilton LD & Meston CM (2013) Chronic stress and sexual function in women. The journal of sexual medicine, 10, 2443– 2454. 23841462 PMC4199300
  52. Hasen NS & Gammie SC (2005) Differential fos activation in virgin and lactating mice in response to an intruder. Physiol Behav, 84, 681– 695. 15885244
  53. Herr NR, Park J, McElligott ZA, Belle AM, Carelli RM & Wightman RM (2012) In vivo voltammetry monitoring of electrically evoked extracellular norepinephrine in subregions of the bed nucleus of the stria terminalis. J Neurophysiol, 107, 1731– 1737. 22190618 PMC3311672
  54. Hess WR (1927) Stammganglien-reizversuche. Verlag Julius Springer.
  55. Hsu Y, Earley RL & Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev Camb Philos Soc, 81, 33– 74. 16460581
  56. Janeček M & Dabrowska J (2019) Oxytocin facilitates adaptive fear and attenuates anxiety responses in animal models and human studies-potential interaction with the corticotropin-releasing factor (CRF) system in the bed nucleus of the stria terminalis (BNST). Cell Tissue Res, 375, 143– 172. 30054732 PMC6336503
  57. Jarrett TM, McMurray MS, Walker CH & Johns JM (2006) Cocaine treatment alters oxytocin receptor binding but not mRNA production in postpartum rat dams. Neuropeptides, 40, 161– 167. 16677710 PMC3109499
  58. Jasnow AM, Davis M & Huhman KL (2004) Involvement of central amygdalar and bed nucleus of the stria terminalis corticotropin-releasing factor in behavioral responses to social defeat. Behav Neurosci, 118, 1052– 1061. 15506887
  59. Johns JM, Noonan LR, Zimmerman LI, Li L & Pedersen CA (1997) Effects of Short- and Long-Term Withdrawal from Gestational Cocaine Treatment on Maternal Behavior and Aggression in Sprague-Dawley Rats. Developmental Neuroscience, 19, 368– 374. 9215883
  60. Kash TL, Pleil KE, Marcinkiewcz CA, Lowery-Gionta EG, Crowley N, Mazzone C, Sugam J, Hardaway JA & McElligott ZA (2015) Neuropeptide regulation of signaling and behavior in the BNST. Mol Cells, 38, 1– 13. 25475545 PMC4314126
  61. Kim Y, Venkataraju KU, Pradhan K, Mende C, Taranda J, Turaga SC, Arganda-Carreras I, Ng L, Hawrylycz MJ & Rockland KS (2015) Mapping social behavior-induced brain activation at cellular resolution in the mouse. Cell reports, 10, 292– 305. 25558063 PMC4294964
  62. Kirn J & Floody OR (1985) Differential effects of lesions in three limbic areas on ultrasound production and lordosis by female hamsters. Behav Neurosci, 99, 1142– 1152. 3843544
  63. Klampfl SM & Bosch OJ (2019) When mothers neglect their offspring: an activated CRF system in the BNST is detrimental for maternal behavior. Arch Womens Ment Health, 22, 409– 415. 30078057
  64. Klampfl SM, Brunton PJ, Bayerl DS & Bosch OJ (2014) Hypoactivation of CRF receptors, predominantly type 2, in the medial-posterior BNST is vital for adequate maternal behavior in lactating rats. J Neurosci, 34, 9665– 9676. 25031406 PMC4099544
  65. Klampfl SM, Brunton PJ, Bayerl DS & Bosch OJ (2016a) CRF-R1 activation in the anterior-dorsal BNST induces maternal neglect in lactating rats via an HPA axis-independent central mechanism. Psychoneuroendocrinology, 64, 89– 98. 26630389 PMC4712652
  66. Klampfl SM, Schramm MM, Stinnett GS, Bayerl DS, Seasholtz AF & Bosch OJ (2016b) Brain CRF-binding protein modulates aspects of maternal behavior under stressful conditions and supports a hypo-anxious state in lactating rats. Horm Behav, 84, 136– 144. 27368148
  67. Kohtz AS, Walf AA & Frye CA (2019a) Effects of non-contingent cocaine on 3 alpha-androstanediol. II. Disruption of lordosis of proestrous rats. Physiol Behav, 203, 113– 119. 29273454
  68. Kohtz AS, Walf AA & Frye CA (2019b) Effects of non-contingent cocaine on 3alpha-androstanediol. I. Disruption of male sexual behavior. Physiol Behav, 203, 120– 127. 29248633
  69. Kono R, Tashiro N & Nakao H (1986) Inhibitory effects of acetylcholine on aggressive-defense reaction induced by electrical stimulation of the hypothalamus in cats. Brain research bulletin, 16, 491– 495. 3719380
  70. Kudo T, Uchigashima M, Miyazaki T, Konno K, Yamasaki M, Yanagawa Y, Minami M & Watanabe M (2012) Three types of neurochemical projection from the bed nucleus of the stria terminalis to the ventral tegmental area in adult mice. J Neurosci, 32, 18035– 18046. 23238719 PMC6621739
  71. Laflamme N, Nappi RE, Drolet G, Labrie C & Rivest S (1998) Expression and neuropeptidergic characterization of estrogen receptors (ERalpha and ERbeta) throughout the rat brain: anatomical evidence of distinct roles of each subtype. J Neurobiol, 36, 357– 378. 9733072
  72. Lebow MA & Chen A (2016) Overshadowed by the amygdala: the bed nucleus of the stria terminalis emerges as key to psychiatric disorders. Mol Psychiatry, 21, 450– 463. 26878891 PMC4804181
  73. Lemos C, Salti A, Amaral IM, Fontebasso V, Singewald N, Dechant G, Hofer A & El Rawas R (2020) Social interaction reward in rats has anti-stress effects. Addiction biology, e12878. 31984611 PMC7757251
  74. Liu YC, Salamone JD & Sachs BD (1997) Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats. J Neurosci, 17, 5245– 5253. 9185562 PMC6573297
  75. Lonstein JS & Gammie SC (2002) Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev, 26, 869– 888. 12667494
  76. Maeda H (1977) Septum and aggression: A review. [Septum and aggression: A review.]. Kyushu Neuro-psychiatry, 23, 7– 16.
  77. Makinson R, Lundgren KH, Seroogy KB & Herman JP (2015) Chronic social subordination stress modulates glutamic acid decarboxylase (GAD) 67 mRNA expression in central stress circuits. Physiology & behavior, 146, 7– 15. 26066725 PMC4598259
  78. Manzano Nieves G, Schilit Nitenson A, Lee HI, Gallo M, Aguilar Z, Johnsen A, Bravo M & Bath KG (2019) Early Life Stress Delays Sexual Maturation in Female Mice. Front Mol Neurosci, 12, 27. 30863281 PMC6399387
  79. Marcinkiewcz CA, Dorrier CE, Lopez AJ & Kash TL (2015) Ethanol induced adaptations in 5-HT2c receptor signaling in the bed nucleus of the stria terminalis: implications for anxiety during ethanol withdrawal. Neuropharmacology, 89, 157– 167. 25229718 PMC4469779
  80. Martinez LA & Petrulis A (2011) The bed nucleus of the stria terminalis is critical for sexual solicitation, but not for opposite-sex odor preference, in female Syrian hamsters. Horm Behav, 60, 651– 659. 21925504 PMC3210388
  81. Martinon D & Dabrowska J (2018) Corticotropin-Releasing Factor Receptors Modulate Oxytocin Release in the Dorsolateral Bed Nucleus of the Stria Terminalis (BNST) in Male Rats. Front Neurosci, 12, 183. 29618970 PMC5871712
  82. Mazzone CM, Pati D, Michaelides M, DiBerto J, Fox JH, Tipton G, Anderson C, Duffy K, McKlveen JM, Hardaway JA, Magness ST, Falls WA, Hammack SE, McElligott ZA, Hurd YL & Kash TL (2018) Acute engagement of G(q)-mediated signaling in the bed nucleus of the stria terminalis induces anxiety-like behavior. Mol Psychiatry, 23, 143– 153. 27956747 PMC5468515
  83. Miczek KA, de Boer SF & Haller J (2013) Excessive aggression as model of violence: a critical evaluation of current preclinical methods. Psychopharmacology (Berl), 226, 445– 458. 23430160 PMC3595336
  84. Miczek KA, DeBold JF, Hwa LS, Newman EL & de Almeida RM (2015) Alcohol and violence: neuropeptidergic modulation of monoamine systems. Ann N Y Acad Sci, 1349, 96– 118. 26285061 PMC4564371
  85. Miczek KA, Maxson SC, Fish EW & Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res, 125, 167– 181. 11682108
  86. Moffitt JR, Bambah-Mukku D, Eichhorn SW, Vaughn E, Shekhar K, Perez JD, Rubinstein ND, Hao J, Regev A, Dulac C & Zhuang X (2018) Molecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region. Science, 362. PMC6482113 30385464
  87. Monga TN, Tan G, Ostermann HJ, Monga U & Grabois M (1998) Sexuality and sexual adjustment of patients with chronic pain. Disabil Rehabil, 20, 317– 329. 9664190
  88. Naik RR & de Jong TR (2017) Transient and persistent behavioral and molecular changes in primiparous female Wistar rats. Eur J Neurosci, 45, 797– 804. 27717050
  89. Nelson CJ, Meter KE, Walker CH, Ayers AA & Johns JM (1998) A Dose–Response Study of Chronic Cocaine on Maternal Behavior in Rats. Neurotoxicology and Teratology, 20, 657– 660. 9831128
  90. Newman EL, Covington HE 3rd, Suh J, Bicakci MB, Ressler KJ, DeBold JF & Miczek KA (2019) Fighting Females: Neural and Behavioral Consequences of Social Defeat Stress in Female Mice. Biol Psychiatry, 86, 657– 668. 31255250 PMC6788975
  91. Ni RJ, Luo PH, Shu YM, Chen JT & Zhou JN (2016) Whole-brain mapping of afferent projections to the bed nucleus of the stria terminalis in tree shrews. Neuroscience, 333, 162– 180. 27436534
  92. Nordman JC, Ma X, Gu Q, Potegal M, Li H, Kravitz AV & Li Z (2020) Potentiation of Divergent Medial Amygdala Pathways Drives Experience-Dependent Aggression Escalation. J Neurosci, 40, 4858– 4880. 32424020 PMC7326350
  93. O’Connell LA & Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol, 519, 3599– 3639. 21800319
  94. Orso R, Creutzberg KC, Wearick-Silva LE, Wendt Viola T, Tractenberg SG, Benetti F & Grassi-Oliveira R (2019) How Early Life Stress Impact Maternal Care: A Systematic Review of Rodent Studies. Frontiers in Behavioral Neuroscience, 13. PMC6724664 31555106
  95. Osakada T, Ishii KK, Mori H, Eguchi R, Ferrero DM, Yoshihara Y, Liberles SD, Miyamichi K & Touhara K (2018) Sexual rejection via a vomeronasal receptor-triggered limbic circuit. Nature Communications, 9, 4463. PMC6203846 30367054
  96. Overstreet DH, Knapp DJ & Breese GR (2002) Accentuated decrease in social interaction in rats subjected to repeated ethanol withdrawals. Alcohol Clin Exp Res, 26, 1259– 1268. 12198403 PMC2865239
  97. Padilla SL, Qiu J, Soden ME, Sanz E, Nestor CC, Barker FD, Quintana A, Zweifel LS, Rønnekleiv OK, Kelly MJ & Palmiter RD (2016) Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state. Nat Neurosci, 19, 734– 741. 27019015 PMC4846501
  98. Pardo-Bellver C, Cádiz-Moretti B, Novejarque A, Martínez-García F & Lanuza E (2012) Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice. Front Neuroanat, 6, 33. 22933993 PMC3423790
  99. Perkins AE, Woodruff ER, Chun LE, Spencer RL, Varlinskaya E & Deak T (2017) Analysis of c-Fos induction in response to social interaction in male and female Fisher 344 rats. Brain Res, 1672, 113– 121. 28764933 PMC5592796
  100. Peyron C, Petit JM, Rampon C, Jouvet M & Luppi PH (1998) Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience, 82, 443– 468. 9466453
  101. Piccin A & Contarino A (2020) Long-lasting pseudo-social aggressive behavior in opiate-withdrawn mice. Prog Neuropsychopharmacol Biol Psychiatry, 97, 109780. 31669507
  102. Pitcher MH, Tarum F, Lehmann M & Bushnell MC (2019) Persistent inflammatory pain alters sexually-motivated behavior in male rats. Behav Brain Res, 356, 380– 389. 30205121 PMC7485009
  103. Potegal M (1992) Time course of aggressive arousal in female hamsters and male rats. Behav Neural Biol, 58, 120– 124. 1456930
  104. Powers JB, Newman SW & Bergondy ML (1987) MPOA and BNST lesions in male Syrian hamsters: differential effects on copulatory and chemoinvestigatory behaviors. Behav Brain Res, 23, 181– 195. 3555537
  105. Rodriguez-Romaguera J, Ung RL, Nomura H, Otis JM, Basiri ML, Namboodiri VM, Zhu X, Robinson JE, McHenry JA, Kosyk O, Jhou TC, Kash TL, Bruchas MR & Stuber GD (2020) Prepronociceptin expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli. bioRxiv, 2020.2001.2021.914341. PMC8136285 33176134
  106. Sajdyk T, Johnson P, Fitz S & Shekhar A (2008) Chronic inhibition of GABA synthesis in the bed nucleus of the stria terminalis elicits anxiety-like behavior. J Psychopharmacol, 22, 633– 641. 18308797 PMC3065212
  107. Shaikh MB, Brutus M, Siegel HE & Siegel A (1986) Regulation of feline aggression by the bed nucleus of stria terminalis. Brain Res Bull, 16, 179– 182. 3697786
  108. Steinman MQ, Laredo SA, Lopez EM, Manning CE, Hao RC, Doig IE, Campi KL, Flowers AE, Knight JK & Trainor BC (2015) Hypothalamic vasopressin systems are more sensitive to the long term effects of social defeat in males versus females. Psychoneuroendocrinology, 51, 122– 134. 25306217 PMC4268083
  109. Todd J, Green G, Harrison M, Ikuesan B, Self C, Pevalin DJ & Baldacchino A (2004) Social exclusion in clients with comorbid mental health and substance misuse problems. Social psychiatry and psychiatric epidemiology, 39, 581– 587. 15243697
  110. Toufexis D (2007) Region- and sex-specific modulation of anxiety behaviours in the rat. J Neuroendocrinol, 19, 461– 473. 17504440
  111. Ungless MA, Singh V, Crowder TL, Yaka R, Ron D & Bonci A (2003) Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron, 39, 401– 407. 12895416
  112. Valzelli L (1973) The “isolation syndrome” in mice. Psychopharmacologia, 31, 305– 320. 4582344
  113. Varlinskaya EI & Spear LP (2015) Social consequences of ethanol: Impact of age, stress, and prior history of ethanol exposure. Physiol Behav, 148, 145– 150. 25431835 PMC4444396
  114. Vasconcelos M, Stein DJ, Albrechet-Souza L, Miczek KA & de Almeida RMM (2019) Recovery of stress-impaired social behavior by an antagonist of the CRF binding protein, CRF(6-33,) in the bed nucleus of the stria terminalis of male rats. Behav Brain Res, 357-358, 104– 110. 29330004 PMC6218317
  115. Vekaria KM, O’Connell K, Rhoads SA, Brethel-Haurwitz KM, Cardinale EM, Robertson EL, Walitt B, VanMeter JW & Marsh AA (2020) Activation in bed nucleus of the stria terminalis (BNST) corresponds to everyday helping. Cortex, 127, 67– 77. 32169677 PMC7239753
  116. Venniro M, Russell TI, Ramsey LA, Richie CT, Lesscher HMB, Giovanetti SM, Messing RO & Shaham Y (2020) Abstinence-dependent dissociable central amygdala microcircuits control drug craving. Proc Natl Acad Sci U S A, 117, 8126– 8134. 32205443 PMC7148559
  117. Venniro M, Zhang M, Caprioli D, Hoots JK, Golden SA, Heins C, Morales M, Epstein DH & Shaham Y (2018) Volitional social interaction prevents drug addiction in rat models. Nat Neurosci, 21, 1520– 1529. 30323276 PMC7386559
  118. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse, 51, 32– 58. 14579424
  119. Welch JD, Kozareva V, Ferreira A, Vanderburg C, Martin C & Macosko EZ (2019) Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity. Cell, 177, 1873– 1887.e1817. 31178122 PMC6716797
  120. Wise RA & Koob GF (2014) The development and maintenance of drug addiction. Neuropsychopharmacology, 39, 254– 262. 24121188 PMC3870778
  121. Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, Honda S, Harada N & Shah NM (2009) Estrogen masculinizes neural pathways and sex-specific behaviors. Cell, 139, 61– 72. 19804754 PMC2851224
  122. Yamamoto R, Ahmed N, Ito T, Gungor NZ & Pare D (2018) Optogenetic Study of Anterior BNST and Basomedial Amygdala Projections to the Ventromedial Hypothalamus. eNeuro, 5. PMC6027956 29971248

Cited by

Sorted by citations

Authors
Flanigan, M. E., & Kash, T. L.
Affiliations
University of North Carolina at Chapel Hill (US)
Corresponding author
Kash, Thomas L.
ORCID
Venue
European Journal of Neuroscience
Publisher
Wiley
Published
2020-11-07
Volume
55
Issue
9-10
Pages
2404-2420
ISSN
  • 0953-816X (ISSN-L)
  • 1460-9568
DOI
10.1111/ejn.14991
PMC
PMC9906816
OpenAlex
W3090191938
Cited by
71
References
27
Citations by year
2026: 9 · 2025: 12 · 2024: 13 · 2023: 19 · 2022: 13 · 2021: 5
FWCI
1.49
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • European Journal of Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
  • UNC Libraries
Funders
National Institute on Alcohol Abuse and Alcoholism (R01 AA011605, R01 AA019454, T32 AA007573‐21)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
bed nucleus of the stria terminalis, social behavior, extended amygdala, sex differences, stress, drugs of abuse, neuropsychiatric disorders, social dysfunction, neural circuits, neuropeptides
MeSH terms
Amygdala, Neuropeptides, Septal Nuclei, Social Behavior

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