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Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions

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Abstract

The impact of paternal care on the development of catecholaminergic fiber innervations in the prefrontal cortex, nucleus accumbens, hippocampus and the amygdala was quantitatively investigated in the biparental Octodon degus. Two age (juvenile, adult) and rearing groups: (1) degus reared without father and (2) degus raised by both parents were compared. Juvenile father-deprived animals showed significantly elevated densities of TH-immunoreactive fibers in all analyzed regions, except in the orbitofrontal cortex, as compared to biparentally reared animals. This difference between the two rearing groups was still evident in adulthood in the prelimbic and infralimbic cortices and in the hippocampal formation. Interestingly, the elevated TH fiber density in both nucleus accumbens subregions was reversed in adulthood, i.e. adult father-deprived animals showed strongly reduced TH fiber densities as compared to biparentally reared animals. We show here that paternal care plays a critical role in the functional maturation of catecholaminergic innervation patterns in prefrontal and limbic brain circuits.

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Abbreviations

Acb:

Nucleus accumbens

AcbC:

Nucleus accumbens, core region

AcbSh:

Nucleus accumbens, shell region

ACd:

Anterior cingulate cortex

BLA:

Basolateral amygdala

CA1:

CA3 subregions of the hippocampal formation

CeA:

Nucleus of the central amygdala

DG:

Dentate gyrus

LO:

Lateral orbitofrontal cortex

OFC:

Orbitofrontal cortex

P:

Postnatal day

PL/IL:

Prelimbic/infralimbic prefrontal cortex

TH:

Tyrosine hydroxylase

VO:

Ventral orbitofrontal cortex

References

  • Akil M, Lewis DA (1993) The dopaminergic innervation of monkey entorhinal cortex. Cereb Cortex 3(6):533–550

    Article  PubMed  CAS  Google Scholar 

  • Amato PR (1994) Father–child relations, mother–child relations, and offspring psychological well-being in early adulthood. J Marriage Fam 56(4):1031–1042

    Article  Google Scholar 

  • Asan E (1993) Comparative single and double immunolabelling with antisera against catecholamine biosynthetic enzymes: criteria for the identification of dopaminergic, noradrenergic and adrenergic structures in selected rat brain areas. Histochemistry 99(6):427–442

    PubMed  CAS  Google Scholar 

  • Bear MF, Singer W (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320(6058):172–176

    Article  PubMed  CAS  Google Scholar 

  • Becker K, Abraham A, Kindler J, Helmeke C, Braun K (2007) Exposure to neonatal separation stress alters exploratory behavior and corticotrophin releasing factor expression in neurons in the amygdala and hippocampus. Dev Neurobiol 67(5):617–629

    Article  PubMed  Google Scholar 

  • Bergstrom HC, McDonald CG, French HT, Smith RF (2008) Continuous nicotine administration produces selective, age-dependent structural alteration of pyramidal neurons from prelimbic cortex. Synapse 62(1):31–39

    Article  PubMed  CAS  Google Scholar 

  • Bienkowski MS, Rinaman L (2011) Immune challenge activates neural inputs to the ventrolateral bed nucleus of the stria terminalis. Physiol Behav 104(2):257–265

    Article  PubMed  CAS  Google Scholar 

  • Blue ME, Parnavelas JG (1982) The effect of neonatal 6-hydroxydopamine treatment on synaptogenesis in the visual cortex of the rat. J Comp Neurol 205(2):199–205

    Article  PubMed  CAS  Google Scholar 

  • Braun K, Lange E, Metzger M, Poeggel G (2000) Maternal separation followed by early social deprivation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus. Neuroscience 95(1):309–318

    Article  PubMed  CAS  Google Scholar 

  • Braun K, Seidel K, Weigel S, Roski C, Poeggel G (2011) Paternal deprivation alters region- and age-specific interneuron expression patterns in the biparental rodent Octodon degus. Cereb Cortex 21(7):1532–1546

    Article  PubMed  Google Scholar 

  • Bredy TW, Lee AW, Meaney MJ, Brown RE (2004) Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus). Horm Behav 46(1):30–38

    Article  PubMed  Google Scholar 

  • Bredy TW, Brown RE, Meaney MJ (2007) Effect of resource availability on biparental care, and offspring neural and behavioral development in the California mouse (Peromyscus californicus). Eur J Neurosci 25(2):567–575

    Article  PubMed  Google Scholar 

  • Brummelte S, Neddens J, Teuchert-Noodt G (2007) Alteration in the GABAergic network of the prefrontal cortex in a potential animal model of psychosis. J Neural Transm 114(5):539–547

    Article  PubMed  CAS  Google Scholar 

  • Busche A, Polascheck D, Lesting J, Neddens J, Teuchert-Noodt G (2004) Developmentally induced imbalance of dopaminergic fibre densities in limbic brain regions of gerbils (Meriones unguiculatus). J Neural Transm 111(4):451–463

    Article  PubMed  CAS  Google Scholar 

  • Cantoni D, Brown RE (1997) Paternal investment and reproductive success in the California mouse, Peromyscus californicus. Anim Behav 54(2):377–386

    Article  PubMed  Google Scholar 

  • Chocyk A, Przyborowska A, Dudys D, Majcher I, Mackowiak M, Wedzony K (2011) The impact of maternal separation on the number of tyrosine hydroxylase-expressing midbrain neurons during different stages of ontogenesis. Neuroscience 182:43–61

    Article  PubMed  CAS  Google Scholar 

  • Colonnello V, Iacobucci P, Fuchs T, Newberry RC, Panksepp J (2011) Octodon degus. A useful animal model for social-affective neuroscience research: basic description of separation distress, social attachments and play. Neurosci Biobehav Rev 35(9):1854–1863

    Article  PubMed  Google Scholar 

  • Crombag HS, Gorny G, Li Y, Kolb B, Robinson TE (2005) Opposite effects of amphetamine self-administration experience on dendritic spines in the medial and orbital prefrontal cortex. Cereb Cortex 15(3):341–348

    Article  PubMed  Google Scholar 

  • Davis M, Falls WA, Campeau S, Kim M (1993) Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 58(1–2):175–198

    Article  PubMed  CAS  Google Scholar 

  • Denys D, Zohar J, Westenberg HG (2004) The role of dopamine in obsessive–compulsive disorder: preclinical and clinical evidence. J Clin Psychiatry 65(Suppl 14):11–17

    PubMed  CAS  Google Scholar 

  • Diaz-Heijtz R, Kolb B, Forssberg H (2003) Can a therapeutic dose of amphetamine during pre-adolescence modify the pattern of synaptic organization in the brain? Eur J Neurosci 18(12):3394–3399

    Article  PubMed  Google Scholar 

  • Ebensperger LA, Ramirez-Otarola N, Leon C, Ortiz ME, Croxatto HB (2010) Early fitness consequences and hormonal correlates of parental behaviour in the social rodent Octodon degus. Physiol Behav 101(4):509–517

    Article  PubMed  CAS  Google Scholar 

  • Elwood RW, Ostermeyer MC (1986) Discrimination between conspecific and allospecific infants by male gerbils and mice before and after experience of their own young. Dev Psychobiol 19(4):327–334

    Article  PubMed  CAS  Google Scholar 

  • Ernst M, Fudge JL (2009) A developmental neurobiological model of motivated behavior: anatomy, connectivity and ontogeny of the triadic nodes. Neurosci Biobehav Rev 33(3):367–382

    Article  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2000) Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology 153(1):17–30

    Article  PubMed  CAS  Google Scholar 

  • Frotscher M, Leranth C (1988) Catecholaminergic innervation of pyramidal and GABAergic nonpyramidal neurons in the rat hippocampus. Double label immunostaining with antibodies against tyrosine hydroxylase and glutamate decarboxylase. Histochemistry 88(3–6):313–319

    PubMed  CAS  Google Scholar 

  • Fudge JL, Emiliano AB (2003) The extended amygdala and the dopamine system: another piece of the dopamine puzzle. J Neuropsychiatry Clin Neurosci 15(3):306–316

    Article  PubMed  CAS  Google Scholar 

  • Gardner EL (2011) Addiction and brain reward and antireward pathways. Adv Psychosom Med 30:22–60

    Article  PubMed  Google Scholar 

  • Gasbarri A, Packard MG, Campana E, Pacitti C (1994a) Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33(4):445–452

    Article  PubMed  CAS  Google Scholar 

  • Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (1994b) Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res 668(1–2):71–79

    Article  PubMed  Google Scholar 

  • Gos T, Becker K, Bock J, Malecki U, Bogerts B, Poeggel G, Braun K (2006) Early neonatal and postweaning social emotional deprivation interferes with the maturation of serotonergic and tyrosine hydroxylase-immunoreactive afferent fiber systems in the rodent nucleus accumbens, hippocampus and amygdala. Neuroscience 140(3):811–821

    Article  PubMed  CAS  Google Scholar 

  • Greba Q, Kokkinidis L (2000) Peripheral and intraamygdalar administration of the dopamine D1 receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle. Behav Neurosci 114(2):262–272

    Article  PubMed  CAS  Google Scholar 

  • Groenewegen HJ, Wright CI, Beijer AV, Voorn P (1999) Convergence and segregation of ventral striatal inputs and outputs. Ann N Y Acad Sci 877:49–63

    Article  PubMed  CAS  Google Scholar 

  • Grossmann K, Grossmann KE, Fremmer-Bombik E, Kindler H, Scheuerer-Englisch H, Zimmermann P (2002) The uniqueness of the child–father attachment relationship: fathers’ sensitive and challenging play as a pivotal variable in a 16-year longitudinal study. Soc Dev 11(3):307–331

    Article  Google Scholar 

  • Guarraci FA, Frohardt RJ, Kapp BS (1999) Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 827(1–2):28–40

    Article  PubMed  CAS  Google Scholar 

  • Harrison AA, Everitt BJ, Robbins TW (1997) Doubly dissociable effects of median- and dorsal-raphe lesions on the performance of the five-choice serial reaction time test of attention in rats. Behav Brain Res 89(1–2):135–149

    Article  PubMed  CAS  Google Scholar 

  • Harsanyi A, Csigo K, Demeter G, Nemeth A (2007) New approach to obsessive–compulsive disorder: dopaminergic theories. Psychiatr Hung 22(4):248–258

    PubMed  Google Scholar 

  • Hasue RH, Shammah-Lagnado SJ (2002) Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat. J Comp Neurol 454(1):15–33

    Article  PubMed  CAS  Google Scholar 

  • Helmeke C, Seidel K, Poeggel G, Bredy TW, Abraham A, Braun K (2009) Paternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus. Neuroscience 163(3):790–798

    Article  PubMed  CAS  Google Scholar 

  • Ikemoto S, Panksepp J (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31(1):6–41

    Article  PubMed  CAS  Google Scholar 

  • Kasamatsu T, Pettigrew JD (1979) Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine. J Comp Neurol 185(1):139–161

    Article  PubMed  CAS  Google Scholar 

  • Kasamatsu T, Pettigrew JD, Ary M (1979) Restoration of visual cortical plasticity by local microperfusion of norepinephrine. J Comp Neurol 185(1):163–181

    Article  PubMed  CAS  Google Scholar 

  • Kim CH, Cheon KA, Koo MS, Ryu YH, Lee JD, Chang JW, Lee HS (2007) Dopamine transporter density in the basal ganglia in obsessive–compulsive disorder, measured with [123I]IPT SPECT before and after treatment with serotonin reuptake inhibitors. Neuropsychobiology 55(3–4):156–162

    Article  PubMed  CAS  Google Scholar 

  • Koob GF (2009) Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56(Suppl 1):18–31

    Article  PubMed  CAS  Google Scholar 

  • Koob GF (2011) Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr Top Behav Neurosci. doi:10.07/7854_2011_129

    Google Scholar 

  • Lamont EW, Kokkinidis L (1998) Infusion of the dopamine D1 receptor antagonist SCH 23390 into the amygdala blocks fear expression in a potentiated startle paradigm. Brain Res 795(1–2):128–136

    Article  PubMed  CAS  Google Scholar 

  • Libhaber N, Eilam D (2002) Social vole parents force their mates to baby-sit. Dev Psychobiol 41(3):236–240

    Article  PubMed  Google Scholar 

  • Lovinger DM (2012) Young investigators stress alcohol-induced neuroadaptations in extended amygdala. Alcohol. doi:10.1016/j.alcohol.2011.11.001

  • Loy R, Koziell DA, Lindsey JD, Moore RY (1980) Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189(4):699–710

    Article  PubMed  CAS  Google Scholar 

  • Metzger M, Jiang S, Wang JZ, Braun K (1996) Organization of the dopaminergic innervation of forebrain areas relevant to learning: a combined immunohistochemical/retrograde tracing study in the domestic chick. J Comp Neurol 376:1–27

    Article  PubMed  CAS  Google Scholar 

  • Moudy AM, Kunkel DD, Schwartzkroin PA (1993) Development of dopamine-beta-hydroxylase-positive fiber innervation of the rat hippocampus. Synapse 15(4):307–318

    Article  PubMed  CAS  Google Scholar 

  • Nader K, Ledoux JE (1999) Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations. Behav Neurosci 113(5):891–901

    Article  PubMed  CAS  Google Scholar 

  • Netter P, Rammsayer T (1991) Reactivity to dopaminergic drugs and aggression related personality traits. Pers Individ Dif 12(10):1009–1017

    Article  Google Scholar 

  • Olivier B, Pattij T, Wood SJ, Oosting R, Sarnyai Z, Toth M (2001) The 5-HT(1A) receptor knockout mouse and anxiety. Behav Pharmacol 12(6–7):439–450

    Article  PubMed  CAS  Google Scholar 

  • Ovtscharoff W Jr, Helmeke C, Braun K (2006) Lack of paternal care affects synaptic development in the anterior cingulate cortex. Brain Res 1116(1):58–63

    Article  PubMed  CAS  Google Scholar 

  • Pare D, Collins DR, Pelletier JG (2002) Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 6(7):306–314

    Article  PubMed  Google Scholar 

  • Paxinos G, Watson C (2006) The rat brain in stereotaxic coordinates. Academic Press, San Diego

  • Perez-Cruz C, Simon M, Czeh B, Flugge G, Fuchs E (2009) Hemispheric differences in basilar dendrites and spines of pyramidal neurons in the rat prelimbic cortex: activity- and stress-induced changes. Eur J Neurosci 29(4):738–747

    Article  PubMed  Google Scholar 

  • Pinkernelle J, Abraham A, Seidel K, Braun K (2009) Paternal deprivation induces dendritic and synaptic changes and hemispheric asymmetry of pyramidal neurons in the somatosensory cortex. Dev Neurobiol 69(10):663–673

    Article  PubMed  Google Scholar 

  • Piovanotti MR, Vieira ML (2004) Presence of the father and parental experience have differentiated effects on pup development in Mongolian gerbils (Meriones unguiculatus). Behav Processes 66(2):107–117

    Article  PubMed  Google Scholar 

  • Robinson TE, Kolb B (1999) Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 11(5):1598–1604

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg DR, Lewis DA (1994) Changes in the dopaminergic innervation of monkey prefrontal cortex during late postnatal development: a tyrosine hydroxylase immunohistochemical study. Biol Psychiatry 36(4):272–277

    Article  PubMed  CAS  Google Scholar 

  • Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 191(3):461–482

    Article  PubMed  CAS  Google Scholar 

  • Samson Y, Wu JJ, Friedman AH, Davis JN (1990) Catecholaminergic innervation of the hippocampus in the cynomolgus monkey. J Comp Neurol 298(2):250–263

    Article  PubMed  CAS  Google Scholar 

  • Schradin C, Pillay N (2004) The striped mouse (Rhabdomys pumilio) from the succulent karoo, South Africa: a territorial group-living solitary forager with communal breeding and helpers at the nest. J Comp Psychol 118(1):37–47

    Article  PubMed  Google Scholar 

  • Seidel K, Poeggel G, Holetschka R, Helmeke C, Braun K (2011) Paternal deprivation affects the development of corticotrophin releasing factor (CRF)-expressing neurons in prefrontal cortex, amygdala and hippocampus of the biparental Octodon degus. J Neuroendocrinol 23(11):1166–1176

    Article  PubMed  CAS  Google Scholar 

  • Sesack SR, Grace AA (2010) Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35(1):27–47

    Article  PubMed  Google Scholar 

  • Smith RJ, Aston-Jones G (2008) Noradrenergic transmission in the extended amygdala: role in increased drug-seeking and relapse during protracted drug abstinence. Brain Struct Funct 213(1–2):43–61

    Article  PubMed  Google Scholar 

  • Sullivan R, Wilson DA, Feldon J, Yee BK, Meyer U, Richter-Levin G, Avi A, Michael T, Gruss M, Bock J, Helmeke C, Braun K (2006) The international society for developmental psychobiology annual meeting symposium: impact of early life experiences on brain and behavioral development. Dev Psychobiol 48(7):583–602

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21(8):323–331

    Article  PubMed  CAS  Google Scholar 

  • Tran-Tu-Yen DA, Marchand AR, Pape JR, Di Scala G, Coutureau E (2009) Transient role of the rat prelimbic cortex in goal-directed behaviour. Eur J Neurosci 30(3):464–471

    Article  PubMed  Google Scholar 

  • van der Kooij MA, Glennon JC (2007) Animal models concerning the role of dopamine in attention-deficit hyperactivity disorder. Neurosci Biobehav Rev 31(4):597–618

    Article  PubMed  Google Scholar 

  • Verney C, Baulac M, Berger B, Alvarez C, Vigny A, Helle KB (1985) Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat. Neuroscience 14(4):1039–1052

    Article  PubMed  CAS  Google Scholar 

  • Vieira ML, Brown RE (2003) Effects of the presence of the father on pup development in California mice (Peromyscus californicus). Dev Psychobiol 42(3):246–251

    Article  PubMed  Google Scholar 

  • Volkow ND, Wang GJ, Kollins SH, Wigal TL, Newcorn JH, Telang F, Fowler JS, Zhu W, Logan J, Ma Y, Pradhan K, Wong C, Swanson JM (2009) Evaluating dopamine reward pathway in ADHD: clinical implications. J Am Med Assoc 302(10):1084–1091

    Article  CAS  Google Scholar 

  • Weinshenker D, Schroeder JP (2007) There and back again: a tale of norepinephrine and drug addiction. Neuropsychopharmacology 32(7):1433–1451

    Article  PubMed  CAS  Google Scholar 

  • Wilson SC (1982) Contact-promoting behavior, social development, and relationship with parents in sibling juvenile degus (Octodon degus). Dev Psychobiol 15(3):257–268

    Article  PubMed  CAS  Google Scholar 

  • Winterfeld KT, Teuchert-Noodt G, Dawirs RR (1998) Social environment alters both ontogeny of dopamine innervation of the medial prefrontal cortex and maturation of working memory in gerbils (Meriones unguiculatus). J Neurosci Res 52(2):201–209

    Article  PubMed  CAS  Google Scholar 

  • Wise RA (2008) Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox Res 14(2–3):169–183

    Article  PubMed  Google Scholar 

  • Wright SL, Brown RE (2002) The importance of paternal care on pup survival and pup growth in Peromyscus californicus when required to work for food. Behav Processes 60(1):41–52

    Article  PubMed  Google Scholar 

  • Wright JW, Kern MD (1992) Stereotaxic atlas of the brain of Octodon degus. J Morphol 214(3):299–320

    Article  PubMed  CAS  Google Scholar 

  • Wynne-Edwards KE (1987) Evidence for obligate monogamy in the djungarian hamster. Phodopus campbelli: pup survival under different parenting conditions. Behav Ecol Sociobiol 20(6):427–437

    Article  Google Scholar 

  • Zahm DS, Grosu S, Irving JC, Williams EA (2003) Discrimination of striatopallidum and extended amygdala in the rat: a role for parvalbumin immunoreactive neurons? Brain Res 978(1–2):141–154

    Article  PubMed  CAS  Google Scholar 

  • Zangrossi H Jr, Viana MB, Zanoveli J, Bueno C, Nogueira RL, Graeff FG (2001) Serotonergic regulation of inhibitory avoidance and one-way escape in the rat elevated T-maze. Neurosci Biobehav Rev 25(7–8):637–645

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by grants from the German-Israeli Foundation (Grant #101/2011), the Center of Brain and Behavioral Sciences (CBBS), the European Regional Development Fund (ERDF) and a postgraduate fellowship from the state of Saxony-Anhalt to K. S.

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Correspondence to Katharina Braun.

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K. Braun and K. Seidel contributed equally to the work.

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Braun, K., Seidel, K., Holetschka, R. et al. Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions. Brain Struct Funct 218, 859–872 (2013). https://doi.org/10.1007/s00429-012-0434-1

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