Paternal deprivation affects the functional maturation of corticotropin-releasing hormone (CRH)- and calbindin-D28k-expressing neurons in the bed nucleus of the stria terminalis (BNST) of the biparental Octodon degus

Brain Structure and Function

Volumn 219, Issue 6, 2014, Pages 1983-1990

  Gos, Tomasz ^a   Schulkin, Jay ^b,c   Gos, Anna ^a,e   Bock, Joerg ^e,f   Poeggel, Gerd ^d   Braun, Katharina ^e,f  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF LEIPZIG   (Germany)

^e OTTO VON GUERICKE UNIVERSITY   (Germany)

^f Center for Brain and Behavioral Sciences (CBBS)   (Germany)

Author keywords

Corticotropin releasing factor; Development; Parental behavior; Quantitative immunocytochemistry

Indexed keywords

CALBINDIN 1; CORTICOTROPIN RELEASING FACTOR;

ANIMAL EXPERIMENT; ARTICLE; BED NUCLEUS OF THE STRIA TERMINALIS; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL DENSITY; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; OCTODON DEGUS; PARENTAL DEPRIVATION; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; ANIMAL; CELL COUNT; CYTOLOGY; METABOLISM; NERVE CELL; OCTODON; PATERNAL BEHAVIOR; SEPTUM NUCLEUS;

ANIMALS; CALBINDIN 1; CELL COUNT; CORTICOTROPIN-RELEASING HORMONE; MALE; NEURONS; OCTODON; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PATERNAL BEHAVIOR; SEPTAL NUCLEI;

EID: 84936153340     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0617-4     Document Type: Article

References (42)

1. Alheid GF (2003) Extended amygdala and basal forebrain. Ann N Y Acad Sci 985:185–205
2. Atzil S, Hendler T, Zagoory-Sharon O, Winetraub Y, Feldman R (2012) Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin. J Am Acad Child Adolesc Psychiatry 51(8):798–811
3. Baimbridge KG, Mody I, Miller JJ (1985) Reduction of rat hippocampal calcium-binding protein following commissural, amygdala, septal, perforant path, and olfactory bulb kindling. Epilepsia 26(5):460–465
4. Blanz B, Geisel B, Laucht M, Esser G, Schmidt MH (1986) Role of the father in the development of school-age children. Results of an epidemiologic study. Z Kinder Jugendpsychiatr 14(1):5–31
5. Bowers G, Cullinan WE, Herman JP (1998) Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J Neurosci 18(15):5938–5947
6. Braun K (1990) Calcium-binding proteins in avian and mammalian central nervous system: localization, development and possible functions. Prog Histochem Cytochem 21(1):1–64
7. Braun K, Scheich H, Braun S, Rogers JH, Heizmann CW (1991) Parvalbumin-, calretinin- and calbindin-D28k-immunoreactivity and GABA in a forebrain region involved in auditory filial imprinting. Brain Res 539(1):31–44
8. 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. doi:10.1093/cercor/bhq208
9. Budefeld T, Grgurevic N, Tobet SA, Majdic G (2008) Sex differences in brain developing in the presence or absence of gonads. Dev Neurobiol 68(7):981–995
10. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35(2):375–475
11. Champagne D, Beaulieu J, Drolet G (1998) CRFergic innervation of the paraventricular nucleus of the rat hypothalamus: a tract-tracing study. J Neuroendocrinol 10(2):119–131
12. Davis M, Shi C (1999) The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Ann N Y Acad Sci 877:281–291
13. Dent G, Choi DC, Herman JP, Levine S (2007) GABAergic circuits and the stress hyporesponsive period in the rat: ontogeny of glutamic acid decarboxylase (GAD) 67 mRNA expression in limbic–hypothalamic stress pathways. Brain Res 1138:1–9. doi:10.1016/j.brainres.2006.04.082
14. Dewsbury DA (1985) Paternal behavior in rodents. Am Zool 25:841–852
15. Dong HW, Swanson LW (2006) Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol 494(1):142–178. doi:10.1002/cne.20788
16. 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
17. Fuchs T, Iacobucci P, MacKinnon KM, Panksepp J (2010) Infant–mother recognition in a social rodent (Octodon degus). J Comp Psychol 124(2):166–175
18. Gilmore RF, Varnum MM, Forger NG (2012) Effects of blocking developmental cell death on sexually dimorphic calbindin cell groups in the preoptic area and bed nucleus of the stria terminalis. Biol Sex Differ 3:5. doi:10.1186/2042-6410-3-5
19. Hammack SE, Roman CW, Lezak KR, Kocho-Shellenberg M, Grimmig B, Falls WA, Braas K, May V (2010) Roles for pituitary adenylate cyclase-activating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J Mol Neurosci 42(3):327–340. doi:10.1007/s12031-010-9364-7
20. Heizmann CW, Braun K (1992) Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends Neurosci 15(7):259–264
21. 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. doi:10.1016/j.neuroscience.2009.07.008
22. Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary–adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29(8):1201–1213
23. Iacopino AM, Christakos S (1990) Corticosterone regulates calbindin-D28k mRNA and protein levels in rat hippocampus. J Biol Chem 265(18):10177–10180
24. Ledoux JE (1995) Emotion: clues from the brain. Annu Rev Psychol 46:209–235
25. Lee Y, Davis M (1997) Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J Neurosci 17(16):6434–6446
26. Lowenstein DH, Miles MF, Hatam F, McCabe T (1991) Up regulation of calbindin-D28K mRNA in the rat hippocampus following focal stimulation of the perforant path. Neuron 6(4):627–633
27. Nagy FZ, Pare D (2008) Timing of impulses from the central amygdala and bed nucleus of the stria terminalis to the brain stem. J Neurophysiol 100(6):3429–3436
28. Narita K, Takei Y, Suda M, Aoyama Y, Uehara T, Kosaka H, Amanuma M, Fukuda M, Mikuni M (2010) Relationship of parental bonding styles with gray matter volume of dorsolateral prefrontal cortex in young adults. Prog Neuropsychopharmacol Biol Psychiatry 34(4):624–631
29. Paxinos G, Watson C (2004) The rat brain in stereotaxic coordinates, vol 5. Elsevier/Academic Press, Amsterdam
30. 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
31. Rosen JB, Schulkin J (1998) From normal fear to pathological anxiety. Psychol Rev 105(2):325–350
32. Schmidt H (2012) Three functional facets of calbindin D-28k. Front Mol Neurosci 5:25. doi:10.3389/fnmol.2012.00025
33. Schradin C, Pillay N (2003) Paternal care in the social and diurnal striped mouse (Rhabdomys pumilio): laboratory and field evidence. J Comp Psychol 117(3):317–324
34. Schulkin J, Morgan MA, Rosen JB (2005) A neuroendocrine mechanism for sustaining fear. Trends Neurosci 28(12):629–635. doi:10.1016/j.tins.2005.09.009
35. Seidel K, Poeggel G, Holetschka R, Helmeke C, Braun K (2011) Paternal deprivation affects the development of corticotrophin-releasing factor-expressing neurones in prefrontal cortex, amygdala and hippocampus of the biparental Octodon degus. J Neuroendocrinol 23(11):1166–1176. doi:10.1111/j.1365-2826.2011.02208.x
36. Sherman PW, Neff BD (2003) Behavioural ecology: father knows best. Nature 425(6954):136–137
37. Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36(3):165–186
38. 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
39. Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463(1–3):199–216
40. Wright JW, Kern MD (1992) Stereotaxic atlas of the brain of Octodon degus. J Morphol 214(3):299–320
41. Wynne-Edwards KE, Lisk RD (1989) Differential effects of paternal presence on pup survival in two species of dwarf hamster (Phodopus sungorus and Phodopus campbelli). Physiol Behav 45(3):465–469
42. Yuan HH, Chen RJ, Zhu YH, Peng CL, Zhu XR (2013) The neuroprotective effect of overexpression of calbindin-D(28k) in an animal model of Parkinson’s disease. Mol Neurobiol 47(1):117–122. doi:10.1007/s12035-012-8332-3