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Published in: Brain Structure and Function 3/2019

Open Access 01-04-2019 | Original Article

Aggression in BALB/cJ mice is differentially predicted by the volumes of anterior and midcingulate cortex

Authors: Sabrina van Heukelum, L. Drost, F. Mogavero, A. Jager, M. N. Havenith, J. C. Glennon

Published in: Brain Structure and Function | Issue 3/2019

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Abstract

Anterior cingulate cortex (ACC) and midcingulate cortex (MCC) have been implicated in the regulation of aggressive behaviour. For instance, patients with conduct disorder (CD) show increased levels of aggression accompanied by changes in ACC and MCC volume. However, accounts of ACC/MCC changes in CD patients have been conflicting, likely due to the heterogeneity of the studied populations. Here, we address these discrepancies by studying volumetric changes of ACC/MCC in the BALB/cJ mouse, a model of aggression, compared to an age- and gender-matched control group of BALB/cByJ mice. We quantified aggression in BALB/cJ and BALB/cByJ mice using the resident–intruder test, and related this to volumetric measures of ACC/MCC based on Nissl-stained coronal brain slices of the same animals. We demonstrate that BALB/cJ behave consistently more aggressively (shorter attack latencies, more frequent attacks, anti-social biting) than the control group, while at the same time showing an increased volume of ACC and a decreased volume of MCC. Differences in ACC and MCC volume jointly predicted a high amount of variance in aggressive behaviour, while regression with only one predictor had a poor fit. This suggests that, beyond their individual contributions, the relationship between ACC and MCC plays an important role in regulating aggressive behaviour. Finally, we show the importance of switching from the classical rodent anatomical definition of ACC as cingulate area 2 and 1 to a definition that includes the MCC and is directly homologous to higher mammalian species: clear behaviour-related differences in ACC/MCC anatomy were only observed using the homologous definition.
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Literature
go back to reference Alegria AA, Radua J, Rubia K (2016) Meta-analysis of fMRI Studies of disruptive behavior disorders. Am J Psychiatry 173:1119–1130CrossRefPubMed Alegria AA, Radua J, Rubia K (2016) Meta-analysis of fMRI Studies of disruptive behavior disorders. Am J Psychiatry 173:1119–1130CrossRefPubMed
go back to reference Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) The anterior cingulate cortex. Ann N Y Acad Sci 935:107–117CrossRefPubMed Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) The anterior cingulate cortex. Ann N Y Acad Sci 935:107–117CrossRefPubMed
go back to reference Amico F, Stauber J, Koutsouleris N, Frodl T (2011) Anterior cingulate cortex gray matter abnormalities in adults with attention deficit hyperactivity disorder: a voxel-based morphometry study. Psychiatry Res Neuroimaging 191:31–35CrossRef Amico F, Stauber J, Koutsouleris N, Frodl T (2011) Anterior cingulate cortex gray matter abnormalities in adults with attention deficit hyperactivity disorder: a voxel-based morphometry study. Psychiatry Res Neuroimaging 191:31–35CrossRef
go back to reference An X, Bandler R, Ongür D, Price JL (1998) Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 401:455–479CrossRefPubMed An X, Bandler R, Ongür D, Price JL (1998) Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J Comp Neurol 401:455–479CrossRefPubMed
go back to reference Bandler R, Keay KA (1996) Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. In: Holstege R, Bandler R, Saper CB (eds) The Emotional motor system. Elsevier, Amsterdam, pp 285–300CrossRef Bandler R, Keay KA (1996) Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. In: Holstege R, Bandler R, Saper CB (eds) The Emotional motor system. Elsevier, Amsterdam, pp 285–300CrossRef
go back to reference Bandler R, Shipley MT (1994) Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 17:379–389CrossRefPubMed Bandler R, Shipley MT (1994) Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci 17:379–389CrossRefPubMed
go back to reference Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300 Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300
go back to reference Boes AD, Tranel D, Anderson SW, Nopoulos P (2008) Right anterior cingulate: a neuroanatomical correlate of aggression and defiance in boys. Behav Neurosci 122:677–684CrossRefPubMedPubMedCentral Boes AD, Tranel D, Anderson SW, Nopoulos P (2008) Right anterior cingulate: a neuroanatomical correlate of aggression and defiance in boys. Behav Neurosci 122:677–684CrossRefPubMedPubMedCentral
go back to reference Bonath B, Tegelbeckers J, Wilke M, Flechtner HH, Krauel K (2016) Regional gray matter volume differences between adolescents with ADHD and typically developing controls: further evidence for anterior cingulate involvement. J Attention Disorders 22:627–638CrossRef Bonath B, Tegelbeckers J, Wilke M, Flechtner HH, Krauel K (2016) Regional gray matter volume differences between adolescents with ADHD and typically developing controls: further evidence for anterior cingulate involvement. J Attention Disorders 22:627–638CrossRef
go back to reference Budhiraja M, Savic I, Lindner P, Jokinen J, Tihonen J, Hodgins S (2017) Brain structure abnormalities in young women who presented conduct disorder in childhood/adolescence. Cogn Affect Behav Neurosci 17:869–885CrossRefPubMedPubMedCentral Budhiraja M, Savic I, Lindner P, Jokinen J, Tihonen J, Hodgins S (2017) Brain structure abnormalities in young women who presented conduct disorder in childhood/adolescence. Cogn Affect Behav Neurosci 17:869–885CrossRefPubMedPubMedCentral
go back to reference Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222CrossRef Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222CrossRef
go back to reference Carmona S, Vilarroya O, Bielsa A et al (2005) Global and regional gray matter reductions in ADHD: a voxel-based morphometric study. Neurosci Lett 389:88–93CrossRefPubMed Carmona S, Vilarroya O, Bielsa A et al (2005) Global and regional gray matter reductions in ADHD: a voxel-based morphometric study. Neurosci Lett 389:88–93CrossRefPubMed
go back to reference Castellanos FX, Sonuga-Barke EJ, Milham MP, Tannock R (2006) Characterizing cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 10:117–123CrossRefPubMed Castellanos FX, Sonuga-Barke EJ, Milham MP, Tannock R (2006) Characterizing cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 10:117–123CrossRefPubMed
go back to reference Chakraborty T, Asok A, Stanton ME, Rosen JB (2016) Variants of contextual fear conditioning induce differential patterns of Egr-1 activity within the young adult prefrontal cortex. Behav Brain Res 302:122–130CrossRefPubMedPubMedCentral Chakraborty T, Asok A, Stanton ME, Rosen JB (2016) Variants of contextual fear conditioning induce differential patterns of Egr-1 activity within the young adult prefrontal cortex. Behav Brain Res 302:122–130CrossRefPubMedPubMedCentral
go back to reference Chen T, Koga K, Descalzi G et al (2014) Postsynaptic potentiation of corticospinal projecting neurons in the anterior cingulate cortex after nerve injury. Molecular Pain 10:33PubMedPubMedCentral Chen T, Koga K, Descalzi G et al (2014) Postsynaptic potentiation of corticospinal projecting neurons in the anterior cingulate cortex after nerve injury. Molecular Pain 10:33PubMedPubMedCentral
go back to reference Comte M, Schön D, Coull JT et al (2014) Dissociating bottom-up and top-down mechanisms in the cortico-limbic system during emotion processing. Cereb Cortex 26:144–155CrossRefPubMed Comte M, Schön D, Coull JT et al (2014) Dissociating bottom-up and top-down mechanisms in the cortico-limbic system during emotion processing. Cereb Cortex 26:144–155CrossRefPubMed
go back to reference De Boer SF, Koolhaas JM (2005) 5-HT1A and 5-HT1B receptor agonists and aggression: a pharmacological challenge of the serotonin deficiency hypothesis. Eur J Pharmacol 526:125–139CrossRefPubMed De Boer SF, Koolhaas JM (2005) 5-HT1A and 5-HT1B receptor agonists and aggression: a pharmacological challenge of the serotonin deficiency hypothesis. Eur J Pharmacol 526:125–139CrossRefPubMed
go back to reference De Brito S, Mechelli A, Wilke M et al (2009) Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain 132:843–852CrossRefPubMed De Brito S, Mechelli A, Wilke M et al (2009) Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain 132:843–852CrossRefPubMed
go back to reference Delevich K, Tucciarone J, Huang ZJ, Li B (2015) The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J Neurosci 35:5743–5753CrossRefPubMedPubMedCentral Delevich K, Tucciarone J, Huang ZJ, Li B (2015) The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J Neurosci 35:5743–5753CrossRefPubMedPubMedCentral
go back to reference Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306CrossRefPubMed Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306CrossRefPubMed
go back to reference Ernst C (2016) Proliferation and differentiation deficits are a major convergence point for neurodevelopmental disorders. Trends Neurosci 39:290–299CrossRefPubMed Ernst C (2016) Proliferation and differentiation deficits are a major convergence point for neurodevelopmental disorders. Trends Neurosci 39:290–299CrossRefPubMed
go back to reference Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93CrossRefPubMed Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93CrossRefPubMed
go back to reference Fairchild G, Hagan CC, Walsh ND, Passamonti L, Calder AJ, Goodyer IM (2013) Brain structure abnormalities in adolescent girls with conduct disorder. J Child Psychol Psychiatry 54:86–95CrossRefPubMed Fairchild G, Hagan CC, Walsh ND, Passamonti L, Calder AJ, Goodyer IM (2013) Brain structure abnormalities in adolescent girls with conduct disorder. J Child Psychol Psychiatry 54:86–95CrossRefPubMed
go back to reference Fairless AH et al (2008) Low sociability is associated with reduced size of the corpus callosum in the BALB/cJ inbred mouse strain. Brain Res 1230:211–217CrossRefPubMedPubMedCentral Fairless AH et al (2008) Low sociability is associated with reduced size of the corpus callosum in the BALB/cJ inbred mouse strain. Brain Res 1230:211–217CrossRefPubMedPubMedCentral
go back to reference Fillinger C, Yalcin I, Barrot M, Veinante P (2017) Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse. Brain Struct Funct 222:1509–1532CrossRefPubMed Fillinger C, Yalcin I, Barrot M, Veinante P (2017) Afferents to anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse. Brain Struct Funct 222:1509–1532CrossRefPubMed
go back to reference Fillinger C, Yalcin I, Barrot M, Veinante P (2018) Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse. Brain Struct Funct 223:1747–1778PubMed Fillinger C, Yalcin I, Barrot M, Veinante P (2018) Efferents of anterior cingulate areas 24a and 24b and midcingulate areas 24a′ and 24b′ in the mouse. Brain Struct Funct 223:1747–1778PubMed
go back to reference Finger EC, Marsh A, Blair KS et al (2012) Impaired functional but preserved structural connectivity in limbic white matter tracts in youth with conduct disorder or oppositional defiant disorder plus psychopathic traits. Psychiatry Res Neuroimaging 202:239–244CrossRef Finger EC, Marsh A, Blair KS et al (2012) Impaired functional but preserved structural connectivity in limbic white matter tracts in youth with conduct disorder or oppositional defiant disorder plus psychopathic traits. Psychiatry Res Neuroimaging 202:239–244CrossRef
go back to reference Gabbott PLA, Warner TA, Jays PRL, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145–177CrossRefPubMed Gabbott PLA, Warner TA, Jays PRL, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145–177CrossRefPubMed
go back to reference Greimel E et al (2013) Changes in grey matter development in autism spectrum disorder. Brain Struct Funct 218:929–942CrossRefPubMed Greimel E et al (2013) Changes in grey matter development in autism spectrum disorder. Brain Struct Funct 218:929–942CrossRefPubMed
go back to reference Herbert MR, Ziegler DA, Makris N et al (2004) Localization of white matter volume increase in autism and developmental language disorder. Ann Neurol 55:530–540CrossRefPubMed Herbert MR, Ziegler DA, Makris N et al (2004) Localization of white matter volume increase in autism and developmental language disorder. Ann Neurol 55:530–540CrossRefPubMed
go back to reference Johansen JP, Fields HL, Manning BH (2001) The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci 98:8077–8082CrossRefPubMed Johansen JP, Fields HL, Manning BH (2001) The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex. Proc Natl Acad Sci 98:8077–8082CrossRefPubMed
go back to reference Kalisch R (2009) The functional neuroanatomy of reappraisal: time matters. Neurosci Biobehav Rev 33:1215–1226CrossRef Kalisch R (2009) The functional neuroanatomy of reappraisal: time matters. Neurosci Biobehav Rev 33:1215–1226CrossRef
go back to reference Kim J, Wasserman EA, Castro L, Freeman JH (2016) Anterior cingulate cortex inactivation impairs rodent visual selective attention and prospective memory. Behav Neurosci 130:75–90CrossRefPubMed Kim J, Wasserman EA, Castro L, Freeman JH (2016) Anterior cingulate cortex inactivation impairs rodent visual selective attention and prospective memory. Behav Neurosci 130:75–90CrossRefPubMed
go back to reference Koike H et al (2016) Chemogenetic inactivation of dorsal anterior cingulate cortex neurons disrupts attentional behavior in mouse. Neuropsychopharmacology 41:1014–1023CrossRefPubMed Koike H et al (2016) Chemogenetic inactivation of dorsal anterior cingulate cortex neurons disrupts attentional behavior in mouse. Neuropsychopharmacology 41:1014–1023CrossRefPubMed
go back to reference Kramer PR, Strand J, Stinson C et al (2017) Role for the ventral posterior medial/posterior lateral thalamus and anterior cingulate cortex in affective/motivation pain induced by varicella zoster virus. Front Integr Neurosci 11:27CrossRefPubMedPubMedCentral Kramer PR, Strand J, Stinson C et al (2017) Role for the ventral posterior medial/posterior lateral thalamus and anterior cingulate cortex in affective/motivation pain induced by varicella zoster virus. Front Integr Neurosci 11:27CrossRefPubMedPubMedCentral
go back to reference Legg CR, Mercier B, Glickstein M (1989) Corticopontine projection in the rat: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 286:427–441CrossRefPubMed Legg CR, Mercier B, Glickstein M (1989) Corticopontine projection in the rat: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol 286:427–441CrossRefPubMed
go back to reference Lin HY, Tseng WYI, Lai MC, Chang YT, Gau SSF (2017) Shared atypical brain anatomy and intrinsic functional architecture in male youth with autism spectrum disorder and their unaffected brothers. Psychol Med 47:639–654CrossRefPubMed Lin HY, Tseng WYI, Lai MC, Chang YT, Gau SSF (2017) Shared atypical brain anatomy and intrinsic functional architecture in male youth with autism spectrum disorder and their unaffected brothers. Psychol Med 47:639–654CrossRefPubMed
go back to reference Liu C, Wang J, Zhan B, Cheng G (2016) Neuronal activity and the expression of hypothalamic oxytocin and vasopressin in social versus cocaine conditioning. Behav Brain Res 310:84–92CrossRefPubMed Liu C, Wang J, Zhan B, Cheng G (2016) Neuronal activity and the expression of hypothalamic oxytocin and vasopressin in social versus cocaine conditioning. Behav Brain Res 310:84–92CrossRefPubMed
go back to reference Marsh AA et al (2013) Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits. J Child Psychol Psychiatry 54:900–910CrossRefPubMedPubMedCentral Marsh AA et al (2013) Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits. J Child Psychol Psychiatry 54:900–910CrossRefPubMedPubMedCentral
go back to reference Matthys W, Lochmann JE (2017) Individual characteristics. In: Matthys W, Lochmann JE (eds) Oppositional defiant disorder and conduct disorder in childhood. Wiley, New Jersey, pp 37–66 Matthys W, Lochmann JE (2017) Individual characteristics. In: Matthys W, Lochmann JE (eds) Oppositional defiant disorder and conduct disorder in childhood. Wiley, New Jersey, pp 37–66
go back to reference McConnell MJ, Moran JV, Abyzov A et al (2017) Intersection of diverse neuronal genomes and neuropsychiatric disease: the brain somatic mosaicism network. Science 356:eaal1641CrossRefPubMedPubMedCentral McConnell MJ, Moran JV, Abyzov A et al (2017) Intersection of diverse neuronal genomes and neuropsychiatric disease: the brain somatic mosaicism network. Science 356:eaal1641CrossRefPubMedPubMedCentral
go back to reference Öngür D, An X, Price JL (1998) Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 401:480–505CrossRefPubMed Öngür D, An X, Price JL (1998) Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 401:480–505CrossRefPubMed
go back to reference Paxinos G, Franklin KBJ (2012) Paxinos and Franklin’s the mouse brain in stereotaxic coordinates, 4th edn. Academic Press, Waltham Paxinos G, Franklin KBJ (2012) Paxinos and Franklin’s the mouse brain in stereotaxic coordinates, 4th edn. Academic Press, Waltham
go back to reference Paxinos G, Watson C (2014) The rat brain in stereotaxic coordinates, 7th edn. Academic Press, Waltham Paxinos G, Watson C (2014) The rat brain in stereotaxic coordinates, 7th edn. Academic Press, Waltham
go back to reference Petrovic P, Castellanos FX (2016) Top-down dysregulation—from ADHD to emotional instability. Front Behav Neurosci 10:70PubMedPubMedCentral Petrovic P, Castellanos FX (2016) Top-down dysregulation—from ADHD to emotional instability. Front Behav Neurosci 10:70PubMedPubMedCentral
go back to reference Rane P, Cochran D, Hodge SM et al (2016) Connectivity in autism: a review of MRI connectivity studies. Harv Rev Psychiatry 23:223–244CrossRef Rane P, Cochran D, Hodge SM et al (2016) Connectivity in autism: a review of MRI connectivity studies. Harv Rev Psychiatry 23:223–244CrossRef
go back to reference Retico A, Giuliano A, Tancredi R et al (2016) The effect of gender on the neuroanatomy of children with autism spectrum disorders: a support vector machine case-control study. Mol Autism 7:5CrossRefPubMedPubMedCentral Retico A, Giuliano A, Tancredi R et al (2016) The effect of gender on the neuroanatomy of children with autism spectrum disorders: a support vector machine case-control study. Mol Autism 7:5CrossRefPubMedPubMedCentral
go back to reference Rogers JC, De Brito SA (2016) Cortical and subcortical gray matter volume in youths with conduct problems. JAMA Psychiatry 73:64–72CrossRef Rogers JC, De Brito SA (2016) Cortical and subcortical gray matter volume in youths with conduct problems. JAMA Psychiatry 73:64–72CrossRef
go back to reference Rushworth MFS, Behrens TEJ, Rudebeck PH, Walton ME (2007) Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour. Trends Cogn Sci 11:168–176CrossRefPubMed Rushworth MFS, Behrens TEJ, Rudebeck PH, Walton ME (2007) Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour. Trends Cogn Sci 11:168–176CrossRefPubMed
go back to reference Seidman LJ, Biederman J, Liang L et al (2011) Gray matter alterations in adults with attention-deficit/hyperactivity disorder identified by voxel based morphometry. Biol Psychiat 69:857–866CrossRefPubMed Seidman LJ, Biederman J, Liang L et al (2011) Gray matter alterations in adults with attention-deficit/hyperactivity disorder identified by voxel based morphometry. Biol Psychiat 69:857–866CrossRefPubMed
go back to reference Shibata H, Naito J (2008) Organization of anterior cingulate and frontal cortical projections to the retrosplenial cortex in the rat. J Comp Neurol 506:30–45CrossRefPubMed Shibata H, Naito J (2008) Organization of anterior cingulate and frontal cortical projections to the retrosplenial cortex in the rat. J Comp Neurol 506:30–45CrossRefPubMed
go back to reference Stevens FL, Hurley RA, Taber KH (2011) Anterior cingulate cortex: unique role in cognition and emotion. J Neuropsychiatry Clin Neurosci 23:121–125CrossRefPubMed Stevens FL, Hurley RA, Taber KH (2011) Anterior cingulate cortex: unique role in cognition and emotion. J Neuropsychiatry Clin Neurosci 23:121–125CrossRefPubMed
go back to reference Tan LL, Pelzer P, Heinl C et al (2017) A pathway from midcingulate cortex to posterior insula gates nociceptive hypersensitivity. Nat Neurosci 20:1591CrossRefPubMed Tan LL, Pelzer P, Heinl C et al (2017) A pathway from midcingulate cortex to posterior insula gates nociceptive hypersensitivity. Nat Neurosci 20:1591CrossRefPubMed
go back to reference Toth M, Tulogdi A, Biro L, Soros P, Mikics E, Haller J (2012) The neural background of hyper-emotional aggression induced by post-weaning social isolation. Behav Brain Res 233:120–129CrossRefPubMed Toth M, Tulogdi A, Biro L, Soros P, Mikics E, Haller J (2012) The neural background of hyper-emotional aggression induced by post-weaning social isolation. Behav Brain Res 233:120–129CrossRefPubMed
go back to reference Van Groen T, Wyss M (2003) Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:249–263CrossRefPubMed Van Groen T, Wyss M (2003) Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:249–263CrossRefPubMed
go back to reference Velez L, Sokoloff G, Miczek KA, Palmer AA, Dulawa SC (2010) Differences in aggressive behavior and DNA copy number variants between BALB/cJ and BALB/cByJ substrains. Behav Genet 40:201–210CrossRefPubMed Velez L, Sokoloff G, Miczek KA, Palmer AA, Dulawa SC (2010) Differences in aggressive behavior and DNA copy number variants between BALB/cJ and BALB/cByJ substrains. Behav Genet 40:201–210CrossRefPubMed
go back to reference Vogt BA (2009) Regions and subregions of the cingulate cortex. In: Vogt BA (ed) Cingulate neurobiology and disease. Oxford University Press, London, pp 3–30 Vogt BA (2009) Regions and subregions of the cingulate cortex. In: Vogt BA (ed) Cingulate neurobiology and disease. Oxford University Press, London, pp 3–30
go back to reference Vogt BA (2014) Cingulate cortex and pain architecture. In: Paxinos G (ed) The rat nervous system, 4th edn. Academic Press, New York, pp 575–596 Vogt BA (2014) Cingulate cortex and pain architecture. In: Paxinos G (ed) The rat nervous system, 4th edn. Academic Press, New York, pp 575–596
go back to reference Vogt BA (2016) Midcingulate cortex: structure, connections, homologies, functions and diseases. J Chem Neuroanat 74:28–46CrossRefPubMed Vogt BA (2016) Midcingulate cortex: structure, connections, homologies, functions and diseases. J Chem Neuroanat 74:28–46CrossRefPubMed
go back to reference Vogt BA (2018) Anxiety and fear from the perspective of cingulate cortex. J Depression Anxiety Forecast 1:1003 Vogt BA (2018) Anxiety and fear from the perspective of cingulate cortex. J Depression Anxiety Forecast 1:1003
go back to reference Vogt BA, Paxinos G (2014) Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct Funct 219:185–192CrossRefPubMed Vogt BA, Paxinos G (2014) Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct Funct 219:185–192CrossRefPubMed
go back to reference Yang PF, Chen DY, Hu JW, Chen JH, Yen CT (2011) Functional tracing of medial nociceptive pathways using activity-dependent manganese-enhanced MRI. Pain 152:194–203CrossRefPubMed Yang PF, Chen DY, Hu JW, Chen JH, Yen CT (2011) Functional tracing of medial nociceptive pathways using activity-dependent manganese-enhanced MRI. Pain 152:194–203CrossRefPubMed
go back to reference Zehle S, Bock J, Jezierski G, Gruss M, Braun K (2007) Methylphenidate treatment recovers stress-induced elevated dendritic spine densities in the rodent dorsal anterior cingulate cortex. Dev Neurobiol 67:1891–1900CrossRefPubMed Zehle S, Bock J, Jezierski G, Gruss M, Braun K (2007) Methylphenidate treatment recovers stress-induced elevated dendritic spine densities in the rodent dorsal anterior cingulate cortex. Dev Neurobiol 67:1891–1900CrossRefPubMed
Metadata
Title
Aggression in BALB/cJ mice is differentially predicted by the volumes of anterior and midcingulate cortex
Authors
Sabrina van Heukelum
L. Drost
F. Mogavero
A. Jager
M. N. Havenith
J. C. Glennon
Publication date
01-04-2019
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-1816-9

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