GABAA receptor signaling in caudal periaqueductal gray regulates maternal aggression and maternal care in mice

Behavioural Brain Research

Volumn 213, Issue 2, 2010, Pages 230-237

  Lee, Grace ^a   Gammie, Stephen C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Bicuculline; Caudal periaqueductal gray (cPAG); Chlordiazepoxide; GABA; Maternal aggression; Maternal behaviors

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; CHLORDIAZEPOXIDE;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FEMALE; LATENT PERIOD; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; MOUSE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; DECISION MAKING; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; INSTITUTE FOR CANCER RESEARCH MOUSE; MICROINJECTION; PHYSIOLOGY;

AGGRESSION; ANIMALS; BICUCULLINE; CHLORDIAZEPOXIDE; CHOICE BEHAVIOR; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; MALE; MATERNAL BEHAVIOR; MICE; MICE, INBRED ICR; MICROINJECTIONS; PERIAQUEDUCTAL GRAY; RECEPTORS, GABA-A; SIGNAL TRANSDUCTION;

EID: 77953912032     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.05.001     Document Type: Article

References (85)

1. Bandler R., McCulloch T., Dreher B. Afferents to a midbrain periaqueductal grey region involved in the 'defence reaction' in the cat as revealed by horseradish peroxidase. I. The telencephalon. Brain Res 1985, 330:109-119.
2. Barbaresi P., Manfrini E. Glutamate decarboxylase-immunoreactive neurons and terminals in the periaqueductal gray of the rat. Neuroscience 1988, 27:183-191.
3. Behbehani M.M. Functional characteristics of the midbrain periaqueductal gray. Prog Neurobiol 1995, 46:575-605.
4. Behbehani M.M., Jiang M.R., Chandler S.D., Ennis M. The effect of GABA and its antagonists on midbrain periaqueductal gray neurons in the rat. Pain 1990, 40:195-204.
5. Bourin M., Hascoet M. The mouse light/dark box test. Eur J Pharmacol 2003, 463:55-65.
6. Bowery N.G., Hudson A.L., Price G.W. GABAA and GABAB receptor site distribution in the rat central nervous system. Neuroscience 1987, 20:365-383.
7. Cameron A.A., Khan I.A., Westlund K.N., Cliffer K.D., Willis W.D. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. I. Ascending projections. J Comp Neurol 1995, 351:568-584.
8. Cameron A.A., Khan I.A., Westlund K.N., Willis W.D. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. II. Descending projections. J Comp Neurol 1995, 351:585-601.
9. Carobrez A.P., Teixeira K.V., Graeff F.G. Modulation of defensive behavior by periaqueductal gray NMDA/glycine-B receptor. Neurosci Biobehav Rev 2001, 25:697-709.
10. Coffield J.A., Bowen K.K., Miletic V. Retrograde tracing of projections between the nucleus submedius, the ventrolateral orbital cortex, and the midbrain in the rat. J Comp Neurol 1992, 321:488-499.
11. D'Anna K.L., Gammie S.C. Activation of corticotropin-releasing factor receptor 2 in lateral septum negatively regulates maternal defense. Behav Neurosci 2009, 123:356-368.
12. D'Anna K.L., Gammie S.C. Hypocretin-1 dose-dependently modulates maternal behaviour in mice. J Endocrinol 2006, 18:1-14.
13. D'Anna K.L., Stevenson S.A., Gammie S.C. Urocortin 1 and 3 impair maternal defense behavior in mice. Behav Neurosci 2005, 161-171.
14. de Almeida R.M., Giovenardi M., da Silva S.P., de Oliveira V.P., Stein D.J. Maternal aggression in Wistar rats: effect of 5-HT2A/2C receptor agonist and antagonist microinjected into the dorsal periaqueductal gray matter and medial septum. Braz J Med Biol Res 2005, 38:597-602.
15. de Almeida R.M., Lucion A.B. 8-OH-DPAT in the median raphe, dorsal periaqueductal gray and corticomedial amygdala nucleus decreases, but in the medial septal area it can increase maternal aggressive behavior in rats. Psychopharmacology (Berl) 1997, 134:392-400.
16. Dean S.R. Diazepam as an adjuvant in clinical psychotherapy. Dis Nerv Syst 1965, 26:181-183.
17. Divac I., Kosmal A., Bjorklund A., Lindvall O. Subcortical projections to the prefrontal cortex in the rat as revealed by the horseradish peroxidase technique. Neuroscience 1978, 3:785-796.
18. Eberhart J.A., Morrell J.I., Krieger M.S., Pfaff D.W. An autoradiographic study of projections ascending from the midbrain central gray, and from the region lateral to it, in the rat. J Comp Neurol 1985, 241:285-310.
19. Ferreira A., Picazo O., Uriarte N., Pereira M., Fernandez-Guasti A. Inhibitory effect of buspirone and diazepam, but not of 8-OH-DPAT, on maternal behavior and aggression. Pharmacol Biochem Behav 2000, 66:389-396.
20. Frye C.A., Edinger K., Sumida K. Androgen administration to aged male mice increases anti-anxiety behavior and enhances cognitive performance. Neuropsychopharmacology 2008, 33:1049-1061.
21. Gammie S.C. Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behav Cogn Neurosci Rev 2005, 4:119-135.
22. Gammie S.C., D'Anna K.L., Gerstein H., Stevenson S.A. Neurotensin inversely modulates maternal aggression. Neuroscience 2009, 158:1215-1223.
23. Gammie S.C., Garland T., Stevenson S.A. Artificial selection for increased maternal defense behavior in mice. Behav Genet 2006, 36:713-722.
24. Gammie S.C., Huang P.L., Nelson R.J. Maternal aggression in endothelial nitric oxide synthase-deficient mice. Horm Behav 2000, 38:13-20.
25. Gammie S.C., Negron A., Newman S.M., Rhodes J.S. Corticotropin releasing factor inhibits maternal aggression in mice. Behav Neurosci 2004, 118:805-814.
26. Gammie S.C., Nelson R.J. cFOS and pCREB activation and maternal aggression in mice. Brain Res 2001, 898:232-241.
27. Gammie S.C., Nelson R.J. Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J Neurosci 1999, 19:8027-8035.
28. Gammie S.C., Stevenson S.A. Effects of daily and acute restraint stress during lactation on maternal aggression and behavior in mice. Stress 2006, 9:171-180.
29. Graeff F.G., Silveira M.C., Nogueira R.L., Audi E.A., Oliveira R.M. Role of the amygdala and periaqueductal gray in anxiety and panic. Behav Brain Res 1993, 58:123-131.
30. Gregg T.R., Siegel A. Brain structures and neurotransmitters regulating aggression in cats: implications for human aggression. Prog Neuropsychopharmacol Biol Psychiatry 2001, 25:91-140.
31. Griebel G., Sanger D.J., Perrault G. Further evidence for differences between non-selective and BZ-1 (omega 1) selective, benzodiazepine receptor ligands in murine models of " state" and " trait" anxiety. Neuropharmacology 1996, 35:1081-1091.
32. Grota L.J., Ader R. Behavior of lactating rats in a dual-chambered maternity cage. Horm Behav 1974, 5:275-282.
33. Harris J.A. Descending antinociceptive mechanisms in the brainstem: their role in the animal's defensive system. J Physiol Paris 1996, 90:15-25.
34. Hasen N.S., Gammie S.C. Maternal aggression: new insights from Egr-1. Brain Res 2006, 1108:147-156.
35. Henderson L.A., Keay K.A., Bandler R. The ventrolateral periaqueductal gray projects to caudal brainstem depressor regions: a functional-anatomical and physiological study. Neuroscience 1998, 82:201-221.
36. Henry B., Vale W., Markou A. The effect of lateral septum corticotropin-releasing factor receptor 2 activation on anxiety is modulated by stress. J Neurosci 2006, 26:9142-9152.
37. Herrero M.T., Insausti R., Gonzalo L.M. Cortically projecting cells in the periaqueductal gray matter of the rat. A retrograde fluorescent tracer study. Brain Res 1991, 543:201-212.
38. Keay K.A., Bandler R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 2001, 25:669-678.
39. Lee G., Gammie S.C. GABA enhancement of maternal defense in mice: possible neural correlates. Pharmacol Biochem Behav 2007, 86:176-187.
40. Lee G., Gammie S.C. GABA(A) receptor signaling in the lateral septum regulates maternal aggression in mice. Behav Neurosci 2009, 123:1169-1177.
41. Lehner P.N. Handbook of ethological methods 1996, Cambridge University Press, Cambridge; New York.
42. Leon M., Woodside B. Energetic limits on reproduction: maternal food intake. Physiol Behav 1983, 30:945-957.
43. Levin R., Stern J.M. Maternal influences on ontogeny of suckling and feeding rhythms in the rat. J Comp Physiol Psychol 1975, 89:711-721.
44. Li Y.Q., Rao Z.R., Shi J.W. Collateral projections from the midbrain periaqueductal gray to the nucleus raphe magnus and nucleus accumbens in the rat. A fluorescent retrograde double-labelling study. Neurosci Lett 1990, 117:285-288.
45. Li Y.Q., Takada M., Matsuzaki S., Shinonaga Y., Mizuno N. Identification of periaqueductal gray and dorsal raphe nucleus neurons projecting to both the trigeminal sensory complex and forebrain structures: a fluorescent retrograde double-labeling study in the rat. Brain Res 1993, 623:267-277.
46. Liu G.X., Cai G.Q., Cai Y.Q., Sheng Z.J., Jiang J., Mei Z., et al. Reduced anxiety and depression-like behaviors in mice lacking GABA transporter subtype 1. Neuropsychopharmacology 2007, 32:1531-1539.
47. Lohman R.J., Liu L., Morris M., O'Brien T.J. Validation of a method for localised microinjection of drugs into thalamic subregions in rats for epilepsy pharmacological studies. J Neurosci Methods 2005, 146:191-197.
48. Lonstein J.S., De Vries G.J. Maternal behaviour in lactating rats stimulates c-fos in glutamate decarboxylase-synthesizing neurons of the medial preoptic area, ventral bed nucleus of the stria terminalis, and ventrocaudal periaqueductal gray. Neuroscience 2000, 100:557-568.
49. Lonstein J.S., Gammie S.C. Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev 2002, 26:869-888.
50. Lonstein J.S., Simmons D.A., Stern J.M. Functions of the caudal periaqueductal gray in lactating rats: kyphosis, lordosis, maternal aggression, and fearfulness. Behav Neurosci 1998, 112:1502-1518.
51. Lonstein J.S., Stern J.M. Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c-fos and electrolytic lesion studies in lactating rats. J Neurosci 1997, 17:3364-3378.
52. Lonstein J.S., Stern J.M. Site and behavioral specificity of periaqueductal gray lesions on postpartum sexual, maternal, and aggressive behaviors in rats. Brain Res 1998, 804:21-35.
53. Mantyh P.W. Connections of midbrain periaqueductal gray in the monkey. I. Ascending efferent projections. J Neurophysiol 1983, 49:567-581.
54. Mantyh P.W. Connections of midbrain periaqueductal gray in the monkey. II. Descending efferent projections. J Neurophysiol 1983, 49:582-594.
55. Mennini T., Gobbi M. Regional distribution of low-affinity GABA receptors coupled to benzodiazepine receptor subtypes in rat brain: an autoradiographic evaluation. Eur J Pharmacol 1990, 189:143-148.
56. Morgan M.M., Whittier K.L., Hegarty D.M., Aicher S.A. Periaqueductal gray neurons project to spinally projecting GABAergic neurons in the rostral ventromedial medulla. Pain 2008, 140:376-386.
57. Mos J., Olivier B. Quantitative and comparative analyses of pro-aggressive actions of benzodiazepines in maternal aggression of rats. Psychopharmacology 1989, 97:152-153.
58. Mos J., Olivier B. RO 15-1788 does not influence postpartum aggression in lactating female rats. Psychopharmacology (Berl) 1986, 90:278-280.
59. Mos J., Olivier B., van Oorschot R. Maternal aggression towards different sized male opponents: effect of chlordiazepoxide treatment of the mothers and d-amphetamine treatment of the intruders. Pharmacol Biochem Behav 1987, 26:577-584.
60. Nicholson C. Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 1985, 333:325-329.
61. Numan M., Numan M.J., Schwarz J.M., Neuner C.M., Flood T.F., Smith C.D. Medial preoptic area interactions with the nucleus accumbens-ventral pallidum circuit and maternal behavior in rats. Behav Brain Res 2005, 158:53-68.
62. Odeh F., Antal M. The projections of the midbrain periaqueductal grey to the pons and medulla oblongata in rats. Eur J Neurosci 2001, 14:1275-1286.
63. Olivier B., Mos J., Oorschot R. Maternal aggression in rats: effects of chlordiazepoxide and fluprazine. Psychopharmacology 1985, 86:68-76.
64. Ottersen O.P. Afferent connections to the amygdaloid complex of the rat with some observations in the cat. III. Afferents from the lower brain stem. J Comp Neurol 1981, 202:335-356.
65. Ottersen O.P., Storm-Mathisen J. Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 1984, 229:374-392.
66. Palanza P., Rodgers R.J., Ferrari P.F., Parmigiani S. Effects of chlordiazepoxide on maternal aggression in mice depend on experience of resident and sex of intruder. Pharmacol Biochem Behav 1996, 54:175-182.
67. Raud S., Innos J., Abramov U., Reimets A., Koks S., Soosaar A., et al. Targeted invalidation of CCK2 receptor gene induces anxiolytic-like action in light-dark exploration, but not in fear conditioning test. Psychopharmacology (Berl) 2005, 181:347-357.
68. Reichling D.B., Basbaum A.I. Contribution of brainstem GABAergic circuitry to descending antinociceptive controls. I. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus. J Comp Neurol 1990, 302:370-377.
69. Reichling D.B., Basbaum A.I. Contribution of brainstem GABAergic circuitry to descending antinociceptive controls. II. Electron microscopic immunocytochemical evidence of GABAergic control over the projection from the periaqueductal gray to the nucleus raphe magnus in the rat. J Comp Neurol 1990, 302:378-393.
70. Rizvi T.A., Ennis M., Behbehani M.M., Shipley M.T. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 1991, 303:121-131.
71. Rizvi T.A., Ennis M., Shipley M.T. Reciprocal connections between the medial preoptic area and the midbrain periaqueductal gray in rat: a WGA-HRP and PHA-L study. J Comp Neurol 1992, 315:1-15.
72. Salzberg H.C., Lonstein J.S., Stern J.M. GABA(A) receptor regulation of kyphotic nursing and female sexual behavior in the caudal ventrolateral periaqueductal gray of postpartum rats. Neuroscience 2002, 114:675-687.
73. Sandner G., Dessort D., Schmitt P., Karli P. Distribution of GABA in the periaqueductal gray matter. Effects of medial hypothalamic lesions. Brain Res 1981, 224:279-290.
74. Shaikh M.B., Siegel A. GABA-mediated regulation of feline aggression elicited from midbrain periaqueductal gray. Brain Res 1990, 507:51-56.
75. Sheehan T.P., Chambers R.A., Russell D.S. Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res Brain Res Rev 2004, 46:71-117.
76. Siegel A., Pott C.B. Neural substrates of aggression and flight in the cat. Prog Neurobiol 1988, 31:261-283.
77. Siegel A., Victoroff J. Understanding human aggression: new insights from neuroscience. Int J Law Psychiatry 2009, 32:209-215.
78. Sieghart W. Pharmacology of benzodiazepine receptors: an update. J Psychiatry Neurosci 1994, 19:24-29.
79. Singewald N., Sharp T. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 2000, 98:759-770.
80. Stern J.M., Levin R. Food availability as a determinant of the rats' circadian rhythm in maternal behavior. Dev Psychobiol 1976, 9:137-148.
81. Svare B., Betteridge C., Katz D., Samuels O. Some situational and experiential determinants of maternal aggression in mice. Physiol Behav 1981, 26:253-258.
82. Van der Horst V.G., Holstege G. Sensory and motor components of reproductive behavior: pathways and plasticity. Behav Brain Res 1998, 92:157-167.
83. Williams F.G., Beitz A.J. Ultrastructural morphometric analysis of GABA-immunoreactive terminals in the ventrocaudal periaqueductal grey: analysis of the relationship of GABA terminals and the GABAA receptor to periaqueductal grey-raphe magnus projection neurons. J Neurocytol 1990, 19:686-696.
84. Yoshimura H., Ogawa N. Acute and chronic effects of psychotropic drugs on maternal aggression in mice. Psychopharmacology (Berl) 1989, 97:339-342.
85. Yoshimura H., Ogawa N. Ethopharmacology of maternal aggression in mice: effects of diazepam and SM-3997. Eur J Pharmacol 1991, 200:147-153.