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

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Abstract

Aggression is a complex behavior that is essential for survival. Of the various forms of aggression, impulsive violent displays without prior planning or deliberation are referred to as affective aggression. Affective aggression is thought to be caused by aberrant perceptions of, and consequent responses to, threat. Understanding the neuronal networks that regulate affective aggression is pivotal to development of novel approaches to treat chronic affective aggression. Here, we provide a detailed anatomical map of neuronal activity in the forebrain of two inbred lines of mice that were selected for low (NC100) and high (NC900) affective aggression. Attack behavior was induced in male NC900 mice by exposure to an unfamiliar male in a novel environment. Forebrain maps of c-Fos+ nuclei, which are surrogates for neuronal activity during behavior, were then generated and analyzed. NC100 males rarely exhibited affective aggression in response to the same stimulus, thus their forebrain c-Fos maps were utilized to identify unique patterns of neuronal activity in NC900s. Quantitative results indicated robust differences in the distribution patterns and densities of c-Fos+ nuclei in distinct thalamic, subthalamic, and amygdaloid nuclei, together with unique patterns of neuronal activity in the nucleus accumbens and the frontal cortices. Our findings implicate these areas as foci regulating differential behavioral responses to an unfamiliar male in NC900 mice when expressing affective aggression. Based on the highly conserved patterns of connections and organization of neuronal limbic structures from mice to humans, we speculate that neuronal activities in analogous networks may be disrupted in humans prone to maladaptive affective aggression.

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References

  • Adolphs R (2010) What does the amygdala contribute to social cognition? Ann NY Acad Sci 1191:42–61

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Barbas H, Rempel-Clower N (1997) Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 7:635–646

    Article  PubMed  CAS  Google Scholar 

  • Barbas H, Zikopoulos B (2007) The prefrontal cortex and flexible behavior. Neuroscientist 13:532–545

    Article  PubMed  Google Scholar 

  • Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69(12):1133–1139

    Article  PubMed  Google Scholar 

  • Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69:1133–1139

    Article  PubMed  Google Scholar 

  • Barlow J (2002) Antenatal anxiety, parenting and behavioural/emotional problems in children. Br J Psychiatry 181:440–441

    Article  PubMed  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Basar K, Sesia T, Groenewegen H, Steinbusch HW, Visser-Vandewalle V, Temel Y (2010) Nucleus accumbens and impulsivity. Prog Neurobiol 92:533–557

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Begic D, Jokic-Begic N (2001) Aggressive behavior in combat veterans with post-traumatic stress disorder. Mil Med 166:671–676

    PubMed  CAS  Google Scholar 

  • Berezovskii VK, Nassi JJ, Born RT (2011) Segregation of feedforward and feedback projections in mouse visual cortex. J Comp Neurol 519:3672–3683

    Article  PubMed  Google Scholar 

  • Blair RJ (2010) Neuroimaging of psychopathy and antisocial behavior: a targeted review. Curr Psychiatry Rep 12:76–82

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bubser M, Deutch AY (1998) Thalamic paraventricular nucleus neurons collateralize to innervate the prefrontal cortex and nucleus accumbens. Brain Res 787:304–310

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Carlezon WA Jr, Devine DP, Wise RA (1995) Habit-forming actions of nomifensine in nucleus accumbens. Psychopharmacology (Berl) 122:194–197

    Article  CAS  Google Scholar 

  • Chorpita BF, Barlow DH (1998) The development of anxiety: the role of control in the early environment. Psychol Bull 124:3–21

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dahlberg LL (1998) Youth violence in the United States. Major trends, risk factors, and prevention approaches. Am J Prev Med 14:259–272

    Article  PubMed  CAS  Google Scholar 

  • Davidson M (2002) What else can we do to combat stigma? World Psychiatry 1:22–23

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13–34

    Article  PubMed  CAS  Google Scholar 

  • Decety J, Porges EC (2011) Imagining being the agent of actions that carry different moral consequences: an fMRI study. Neuropsychologia 49:2994–3001

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dierick HA, Greenspan RJ (2006) Molecular analysis of flies selected for aggressive behavior. Nat Genet 38:1023–1031

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Dolan RJ (2007) The human amygdala and orbital prefrontal cortex in behavioural regulation. Philos Trans R Soc Lond B Biol Sci 362:787–799

    Article  PubMed  CAS  Google Scholar 

  • Dolan MC (2010) What imaging tells us about violence in anti-social men. Crim Behav Ment Health 20:199–214

    Article  PubMed  Google Scholar 

  • Edwards DA, Isaacs S (1991) Zona incerta lesions: effects on copulation, partner-preference and other socio-sexual behaviors. Behav Brain Res 44:145–150

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Graybiel AM (2008) Habits, rituals, and the evaluative brain. Annu Rev Neurosci 31:359–387

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hasen NS, Gammie SC (2005) Differential fos activation in virgin and lactating mice in response to an intruder. Physiol Behav 84:681–695

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Joiner TE Jr (1996) The relations of thematic and nonthematic childhood depression measures to defensiveness and gender. J Abnorm Child Psychol 24:803–813

    Article  PubMed  Google Scholar 

  • Kalivas PW (2009) The glutamate homeostasis hypothesis of addiction. Nat Rev Neurosci 10:561–572

    Article  PubMed  CAS  Google Scholar 

  • Kalivas PW, McFarland K (2003) Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl) 168:44–56

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Koenigs M, Grafman J (2009) Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15:540–548

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Krug EG, Mercy JA, Dahlberg LL, Zwi AB (2002) The world report on violence and health. Lancet 360:1083–1088

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Martin KA (2011) Neuroanatomy: uninhibited connectivity in neocortex? Curr Biol 21:R425–R427

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Garcia F, Novejarque A, Lanuza E (2008) Two interconnected functional systems in the amygdala of amniote vertebrates. Brain Res Bull 75:206–213

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pare D, Quirk GJ, LeDoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1–9

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Price JL (2003) Comparative aspects of amygdala connectivity. Ann NY Acad Sci 985:50–58

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Redgrave P, Prescott TJ, Gurney K (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009–1023

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Robbins TW, Ersche KD, Everitt BJ (2008) Drug addiction and the memory systems of the brain. Ann NY Acad Sci 1141:1–21

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues SM, LeDoux JE, Sapolsky RM (2009) The influence of stress hormones on fear circuitry. Annu Rev Neurosci 32:289–313

    Article  PubMed  CAS  Google Scholar 

  • Samson RD, Pare D (2005) Activity-dependent synaptic plasticity in the central nucleus of the amygdala. J Neurosci 25:1847–1855

    Article  PubMed  CAS  Google Scholar 

  • Samson RD, Dumont EC, Pare D (2003) Feedback inhibition defines transverse processing modules in the lateral amygdala. J Neurosci 23:1966–1973

    PubMed  CAS  Google Scholar 

  • Samson RD, Duvarci S, Pare D (2005) Synaptic plasticity in the central nucleus of the amygdala. Rev Neurosci 16:287–302

    PubMed  Google Scholar 

  • Sandnabba NK (1996) Selective breeding for isolation-induced intermale aggression in mice: associated responses and environmental influences. Behav Genet 26:477–488

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sellings LH, Clarke PB (2003) Segregation of amphetamine reward and locomotor stimulation between nucleus accumbens medial shell and core. J Neurosci 23:6295–6303

    PubMed  CAS  Google Scholar 

  • Sesack SR, Grace AA (2010) Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27–47

    Article  PubMed  Google Scholar 

  • Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169–191

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Siegel A, Roeling TA, Gregg TR, Kruk MR (1999) Neuropharmacology of brain-stimulation-evoked aggression. Neurosci Biobehav Rev 23:359–389

    Article  PubMed  CAS  Google Scholar 

  • Sotres-Bayon F, Quirk GJ (2010) Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol 20:231–235

    Article  PubMed  CAS  Google Scholar 

  • Soyka M (2011) Neurobiology of aggression and violence in schizophrenia. Schizophr Bull 37:913–920

    Article  PubMed  Google Scholar 

  • Stein DJ, Hollander E, DeCaria C, Trungold S (1991) OCD: a disorder with anxiety, aggression, impulsivity, and depressed mood. Psychiatry Res 36:237–239

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW (2003) The amygdala and its place in the cerebral hemisphere. Ann N Y Acad Sci 985:174–184

    Article  PubMed  Google Scholar 

  • Teicher JD (1972) The alienated, older, isolated male adolescent. Am J Psychother 26:401–407

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Urbain N, Deschenes M (2007) Motor cortex gates vibrissal responses in a thalamocortical projection pathway. Neuron 56:714–725

    Article  PubMed  CAS  Google Scholar 

  • van Oortmerssen GA, Bakker TC (1981) Artificial selection for short and long attack latencies in wild Mus musculus domesticus. Behav Genet 11:115–126

    Article  PubMed  Google Scholar 

  • Van Praag HM (2001) Anxiety/aggression-driven depression. A paradigm of functionalization and verticalization of psychiatric diagnosis. Prog Neuropsychopharmacol Biol Psychiatry 25:893–924

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Wang L, Anderson DJ (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463:227–231

    Article  PubMed  CAS  Google Scholar 

  • West MJ, Gundersen HJ (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1–22

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Samina Ali, Mohamed Hammad, Blair Therit, and Raul Salinas provided excellent technical support. We thank Dr. Jean Lauder at UNC-Chapel Hill for use of her laboratory at the initial stages of this project. We thank Drs. Frank Longo and Rick Meeker for providing us with the use of their StereoInvestigator Software. We apologize to the large number of investigators whose primary work on this topic could not be cited due to space limitations. This work was supported by institutional funds to HTG.

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The authors declare that they have no conflict of interest.

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  1. Department of Molecular Biomedical Sciences and Center for Comparative Medicine and Translational Research, College of Veterinary Medicine, North Carolina State University, 1060 William Moore Dr, Raleigh, NC, 27607, USA

    Derrick L. Nehrenberg, Atif Sheikh & H. Troy Ghashghaei

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  1. Derrick L. Nehrenberg
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Correspondence to H. Troy Ghashghaei.

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Nehrenberg, D.L., Sheikh, A. & Ghashghaei, H.T. Identification of neuronal loci involved with displays of affective aggression in NC900 mice. Brain Struct Funct 218, 1033–1049 (2013). https://doi.org/10.1007/s00429-012-0445-y

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