Identification of neuronal loci involved with displays of affective aggression in NC900 mice

Brain Structure and Function

Volumn 218, Issue 4, 2013, Pages 1033-1049

  Nehrenberg, Derrick L ^a   Sheikh, Atif ^a   Ghashghaei, H Troy ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Aggression; Amygdala; Anxiety disorders; c Fos; Hypothalamus; Limbic thalamus; Mouse; Neural networks; Neuronal activity; Neuronal circuits; Nucleus accumbens; Parafascicular thalamic nucleus; Paraventricular thalamic nucleus; Violence; Zona incerta

Indexed keywords

PROTEIN C FOS;

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CONTROLLED STUDY; FOREBRAIN; FRONTAL CORTEX; INBRED STRAIN; MALE; MOUSE; NERVE CELL NETWORK; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SUBTHALAMUS; THALAMUS;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; BRAIN MAPPING; CELL COUNT; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED STRAINS; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; NEURONS; PROSENCEPHALON; PROTO-ONCOGENE PROTEINS C-FOS;

MUS;

EID: 84879799037     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-012-0445-y     Document Type: Article

References (109)

1. Adolphs R (2010) What does the amygdala contribute to social cognition? Ann NY Acad Sci 1191:42-61
2. Alexander GE, Crutcher MD, DeLong MR (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 85:119-146
3. Alia-Klein N, Goldstein RZ, Tomasi D, Woicik PA, Moeller SJ, Williams B, Craig IW, Telang F, Biegon A, Wang GJ, Fowler JS, Volkow ND (2009) Neural mechanisms of anger regulation as a function of genetic risk for violence. Emotion 9:385-396
4. Barbas H, Rempel-Clower N (1997) Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 7:635-646
5. Barbas H, Zikopoulos B (2007) The prefrontal cortex and flexible behavior. Neuroscientist 13:532-545
6. Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69(12):1133-1139
7. Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69:1133-1139
8. Barlow J (2002) Antenatal anxiety, parenting and behavioural/emotional problems in children. Br J Psychiatry 181:440-441
9. Bartolomucci A, Fucks E, Koolhass JM, Ohl F (2009) Acute and chronic social defeat: stress protocols and behavioral testing. In: Gould TD (ed) Mood and anxiety related phenotypes in mice. Humana Press, New York, pp 261-275
10. Basar K, Sesia T, Groenewegen H, Steinbusch HW, Visser-Vandewalle V, Temel Y (2010) Nucleus accumbens and impulsivity. Prog Neurobiol 92:533-557
11. Beckham JC, Feldman ME, Kirby AC, Hertzberg MA, Moore SD (1997) Interpersonal violence and its correlates in Vietnam veterans with chronic posttraumatic stress disorder. J Clin Psychol 53:859-869
12. Begic D, Jokic-Begic N (2001) Aggressive behavior in combat veterans with post-traumatic stress disorder. Mil Med 166:671-676
13. Berezovskii VK, Nassi JJ, Born RT (2011) Segregation of feedforward and feedback projections in mouse visual cortex. J Comp Neurol 519:3672-3683
14. Blair RJ (2010) Neuroimaging of psychopathy and antisocial behavior: a targeted review. Curr Psychiatry Rep 12:76-82
15. Brown HD, Baker PM, Ragozzino ME (2010) The parafascicular thalamic nucleus concomitantly influences behavioral flexibility and dorsomedial striatal acetylcholine output in rats. J Neurosci 30:14390-14398
16. Bubser M, Deutch AY (1998) Thalamic paraventricular nucleus neurons collateralize to innervate the prefrontal cortex and nucleus accumbens. Brain Res 787:304-310
17. Bubser M, Deutch AY (1999) Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites. Synapse 32:13-22
18. Cairns RB, MacCombie DJ, Hood KE (1983) A developmental-genetic analysis of aggressive behavior in mice: i behavioral outcomes. J Comp Psychol 97:69-89
19. Carlezon WA Jr, Devine DP, Wise RA (1995) Habit-forming actions of nomifensine in nucleus accumbens. Psychopharmacology (Berl) 122:194-197
20. Chorpita BF, Barlow DH (1998) The development of anxiety: the role of control in the early environment. Psychol Bull 124:3-21
21. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Muller C, Luthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277-282
22. Comoli E, Ribeiro-Barbosa ER, Negrao N, Goto M, Canteras NS (2005) Functional mapping of the prosencephalic systems involved in organizing predatory behavior in rats. Neuroscience 130:1055-1067
23. Dahlberg LL (1998) Youth violence in the United States. Major trends, risk factors, and prevention approaches. Am J Prev Med 14:259-272
24. Davidson M (2002) What else can we do to combat stigma? World Psychiatry 1:22-23
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
26. Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13-34
27. Decety J, Porges EC (2011) Imagining being the agent of actions that carry different moral consequences: an fMRI study. Neuropsychologia 49:2994-3001
28. Del Arco A, Mora F (2009) Neurotransmitters and prefrontal cortex-limbic system interactions: implications for plasticity and psychiatric disorders. J Neural Transm 116:941-952
29. Dierick HA, Greenspan RJ (2006) Molecular analysis of flies selected for aggressive behavior. Nat Genet 38:1023-1031
30. Dodge KA, Lansford JE, Burks VS, Bates JE, Pettit GS, Fontaine R, Price JM (2003) Peer rejection and social information-processing factors in the development of aggressive behavior problems in children. Child Dev 74:374-393
31. Dolan RJ (2007) The human amygdala and orbital prefrontal cortex in behavioural regulation. Philos Trans R Soc Lond B Biol Sci 362:787-799
32. Dolan MC (2010) What imaging tells us about violence in anti-social men. Crim Behav Ment Health 20:199-214
33. Edwards DA, Isaacs S (1991) Zona incerta lesions: effects on copulation, partner-preference and other socio-sexual behaviors. Behav Brain Res 44:145-150
34. Edwards AC, Zwarts L, Yamamoto A, Callaerts P, Mackay TF (2009) Mutations in many genes affect aggressive behavior in Drosophila melanogaster. BMC Biol 7:29
35. Erling A, Wiklun I, Albertsson WK (2002) Psychological functioning in boys of short stature: effects of different levels of growth hormone secretion. Acta Paediatr 91:966-971
36. Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85-93
37. Feger J, Bevan M, Crossman AR (1994) The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: a comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study. Neuroscience 60:125-132
38. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47
39. Foland-Ross LC, Altshuler LL, Bookheimer SY, Lieberman MD, Townsend J, Penfold C, Moody T, Ahlf K, Shen JK, Madsen SK, Rasser PE, Toga AW, Thompson PM (2010) Amygdala reactivity in healthy adults is correlated with prefrontal cortical thickness. J Neurosci 30:16673-16678
40. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145-177
41. Gariepy JL, Rodriguiz RM, Jones BC (2002) Handling, genetic and housing effects on the mouse stress system, dopamine function, and behavior. Pharmacol Biochem Behav 73:7-17
42. Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261-1279
43. Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34:905-923
44. Graybiel AM (2008) Habits, rituals, and the evaluative brain. Annu Rev Neurosci 31:359-387
45. Halasz J, Liposits Z, Kruk MR, Haller J (2002) Neural background of glucocorticoid dysfunction-induced abnormal aggression in rats: involvement of fear- and stress-related structures. Eur J Neurosci 15:561-569
46. Haller J, Toth 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
47. Hasen NS, Gammie SC (2005) Differential fos activation in virgin and lactating mice in response to an intruder. Physiol Behav 84:681-695
48. Heise CE, Mitrofanis J (2004) Evidence for a glutamatergic projection from the zona incerta to the basal ganglia of rats. J Comp Neurol 468:482-495
49. Hooks BM, Hires SA, Zhang YX, Huber D, Petreanu L, Svoboda K, Shepherd GM (2011) Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol 9:e1000572
50. Hsu DT, Price JL (2009) Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 512:825-848
51. Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27-78
52. Joiner TE Jr (1996) The relations of thematic and nonthematic childhood depression measures to defensiveness and gender. J Abnorm Child Psychol 24:803-813
53. Kalivas PW (2009) The glutamate homeostasis hypothesis of addiction. Nat Rev Neurosci 10:561-572
54. Kalivas PW, McFarland K (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl) 168:44-56
55. Katzel D, Zemelman BV, Buetfering C, Wolfel M, Miesenbock G (2011) The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat Neurosci 14:100-107
56. Klumpers F, Raemaekers MA, Ruigrok AN, Hermans EJ, Kenemans JL, Baas JM (2010) Prefrontal mechanisms of fear reduction after threat offset. Biol Psychiatry 68:1031-1038
57. Koenigs M, Grafman J (2009) Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15:540-548
58. Koh KB, Kim DK, Kim SY, Park JK (2005) The relation between anger expression, depression, and somatic symptoms in depressive disorders and somatoform disorders. J Clin Psychiatry 66:485-491
59. Krug EG, Mercy JA, Dahlberg LL, Zwi AB (2002) The world report on violence and health. Lancet 360:1083-1088
60. Lanius RA, Vermetten E, Loewenstein RJ, Brand B, Schmahl C, Bremner JD, Spiegel D (2010) Emotion modulation in PTSD: clinical and neurobiological evidence for a dissociative subtype. Am J Psychiatry 167:640-647
61. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184
62. Lightowler S, Kennett GA, Williamson IJ, Blackburn TP, Tulloch IF (1994) Anxiolytic-like effect of paroxetine in a rat social interaction test. Pharmacol Biochem Behav 49:281-285
63. Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221-226
64. Martin KA (2011) Neuroanatomy: uninhibited connectivity in neocortex? Curr Biol 21:R425-R427
65. Martinez-Garcia F, Novejarque A, Lanuza E (2008) Two interconnected functional systems in the amygdala of amniote vertebrates. Brain Res Bull 75:206-213
66. Masri R, Quiton RL, Lucas JM, Murray PD, Thompson SM, Keller A (2009) Zona incerta: a role in central pain. J Neurophysiol 102:181-191
67. Miczek KA, de Almeida RM, Kravitz EA, Rissman EF, de Boer SF, Raine A (2007) Neurobiology of escalated aggression and violence. J Neurosci 27:11803-11806
68. Minamimoto T, Hori Y, Kimura M (2009) Roles of the thalamic CM-PF complex-basal ganglia circuit in externally driven rebias of action. Brain Res Bull 78:75-79
69. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381-425
70. Morgan JI, Cohen DR, Hempstead JL, Curran T (1987) Mapping patterns of c-Fos expression in the central nervous system after seizure. Science 237:192-197
71. Murray EA, Wise SP (2010) Interactions between orbital prefrontal cortex and amygdala: advanced cognition, learned responses and instinctive behaviors. Curr Opin Neurobiol 20:212-220
72. Nehrenberg DL, Rodriguiz RM, Cyr M, Zhang X, Lauder JM, Gariepy JL, Wetsel WC (2009) An anxiety-like phenotype in mice selectively bred for aggression. Behav Brain Res 201:179-191
73. Nehrenberg DL, Wang S, Buus RJ, Perkins J, de Villena FP, Pomp D (2010) Genomic mapping of social behavior traits in a F2 cross derived from mice selectively bred for high aggression. BMC Genet 11:113
74. Pan Y, Xu L, Young KA, Wang Z, Zhang Z (2010) Agonistic encounters and brain activation in dominant and subordinate male greater long-tailed hamsters. Horm Behav 58:478-484
75. Pardini M, Krueger F, Hodgkinson C, Raymont V, Ferrier C, Goldman D, Strenziok M, Guida S, Grafman J (2011) Prefrontal cortex lesions and MAO-A modulate aggression in penetrating traumatic brain injury. Neurology 76:1038-1045
76. Pare D, Quirk GJ, LeDoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1-9
77. Passamonti L, Crockett MJ, Apergis-Schoute AM, Clark L, Rowe JB, Calder AJ, Robbins TW (2012) Effects of acute tryptophan depletion on prefrontal-amygdala connectivity while viewing facial signals of aggression. Biol Psychiatry 71:36-43
78. Peng ZC, Bentivoglio M (2004) The thalamic paraventricular nucleus relays information from the suprachiasmatic nucleus to the amygdala: a combined anterograde and retrograde tracing study in the rat at the light and electron microscopic levels. J Neurocytol 33:101-116
79. Pinto A, Jankowski M, Sesack SR (2003) Projections from the paraventricular nucleus of the thalamus to the rat prefrontal cortex and nucleus accumbens shell: ultrastructural characteristics and spatial relationships with dopamine afferents. J Comp Neurol 459:142-155
80. Price JL (2003) Comparative aspects of amygdala connectivity. Ann NY Acad Sci 985:50-58
81. Rassnick S, Hoffman GE, Rabin BS, Sved AF (1998) Injection of corticotropin-releasing hormone into the locus coeruleus or foot shock increases neuronal Fos expression. Neuroscience 85:259-268
82. Redgrave P, Prescott TJ, Gurney K (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009-1023
83. Reynolds SM, Zahm DS (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25:11757-11767
84. Robbins TW, Ersche KD, Everitt BJ (2008) Drug addiction and the memory systems of the brain. Ann NY Acad Sci 1141:1-21
85. Rodd-Henricks ZA, McKinzie DL, Li TK, Murphy JM, McBride WJ (2002) Cocaine is self-administered into the shell but not the core of the nucleus accumbens of Wistar rats. J Pharmacol Exp Ther 303:1216-1226
86. Rodrigues SM, LeDoux JE, Sapolsky RM (2009) The influence of stress hormones on fear circuitry. Annu Rev Neurosci 32:289-313
87. Samson RD, Pare D (2005) Activity-dependent synaptic plasticity in the central nucleus of the amygdala. J Neurosci 25:1847-1855
88. Samson RD, Dumont EC, Pare D (2003) Feedback inhibition defines transverse processing modules in the lateral amygdala. J Neurosci 23:1966-1973
89. Samson RD, Duvarci S, Pare D (2005) Synaptic plasticity in the central nucleus of the amygdala. Rev Neurosci 16:287-302
90. Sandnabba NK (1996) Selective breeding for isolation-induced intermale aggression in mice: associated responses and environmental influences. Behav Genet 26:477-488
91. Schiffer B, Muller BW, Scherbaum N, Hodgins S, Forsting M, Wiltfang J, Gizewski ER, Leygraf N (2011) Disentangling structural brain alterations associated with violent behavior from those associated with substance use disorders. Arch Gen Psychiatry 68:1039-1049
92. Sellings LH, Clarke PB (2003) Segregation of amphetamine reward and locomotor stimulation between nucleus accumbens medial shell and core. J Neurosci 23:6295-6303
93. Sesack SR, Grace AA (2010) Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27-47
94. Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169-191
95. Shumyatsky GP, Malleret G, Shin RM, Takizawa S, Tully K, Tsvetkov E, Zakharenko SS, Joseph J, Vronskaya S, Yin D, Schubart UK, Kandel ER, Bolshakov VY (2005) Stathmin, a gene enriched in the amygdala, controls both learned and innate fear. Cell 123:697-709
96. Siegel A, Roeling TA, Gregg TR, Kruk MR (1999) Neuropharmacology of brain-stimulation-evoked aggression. Neurosci Biobehav Rev 23:359-389
97. Sotres-Bayon F, Quirk GJ (2010) Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol 20:231-235
98. Soyka M (2011) Neurobiology of aggression and violence in schizophrenia. Schizophr Bull 37:913-920
99. Stein DJ, Hollander E, DeCaria C, Trungold S (1991) OCD: a disorder with anxiety, aggression, impulsivity, and depressed mood. Psychiatry Res 36:237-239
100. Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, Kempadoo KA, Zhang F, Deisseroth K, Bonci A (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:377-380
101. Swanson LW (2003) The amygdala and its place in the cerebral hemisphere. Ann N Y Acad Sci 985:174-184
102. Teicher JD (1972) The alienated, older, isolated male adolescent. Am J Psychother 26:401-407
103. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358-362
104. Urbain N, Deschenes M (2007) Motor cortex gates vibrissal responses in a thalamocortical projection pathway. Neuron 56:714-725
105. van Oortmerssen GA, Bakker TC (1981) Artificial selection for short and long attack latencies in wild Mus musculus domesticus. Behav Genet 11:115-126
106. Van Praag HM (2001) Anxiety/aggression-driven depression. A paradigm of functionalization and verticalization of psychiatric diagnosis. Prog Neuropsychopharmacol Biol Psychiatry 25:893-924
107. Vogt BA, Hof PR, Friedman DP, Sikes RW, Vogt LJ (2008) Norepinephrinergic afferents and cytology of the macaque monkey midline, mediodorsal, and intralaminar thalamic nuclei. Brain Struct Funct 212:465-479
108. Wang L, Anderson DJ (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463:227-231
109. West MJ, Gundersen HJ (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1-22