Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats

Synapse

Volumn 68, Issue 2, 2014, Pages 61-72

  Koss, Wendy A ^a   Belden, Chelsea E ^a   Hristov, Alexander D ^a   Juraska, Janice M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Adolescence; Dendrite; Dendritic spines; Golgi, synapse; Puberty; Sex differences

Indexed keywords

ADDICTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; DENDRITIC CELL; DENDRITIC SPINE; FEMALE; GOLGI STAIN; MALE; MEDIAL PREFRONTAL CORTEX; MENTAL DISEASE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ADOLESCENCE; DENDRITE; DENDRITIC SPINES; GOLGI, SYNAPSE; PUBERTY; SEX DIFFERENCES;

AMYGDALA; ANIMALS; DENDRITIC SPINES; FEMALE; MALE; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RATS, LONG-EVANS; SEX FACTORS;

EID: 84890131267     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21716     Document Type: Article

References (72)

1. Amaral DG. 1986. Amygdalohippocampal and amygdalocortical projections in the primate brain. Adv Exp Med Biol 203:3-17.
2. Anderson SA, Classey JD, Conde F, Lund JS, Lewis DA. 1995. Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience 67:7-22.
3. Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH. 2000. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167-169.
4. Anderson VA, Anderson P, Northam E, Jacobs R, Catroppa C. 2001. Development of executive functions through late childhood and adolescence in an australian sample. Dev Neuropsychol 20:385-406.
5. Andersen SL, Thompson AP, Krenzel E, Teicher MH. 2002. Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology 27:683-691.
6. Benes FM, Gisabella B. 2006. Rat modeling for GABA defects in schizophrenia. Adv Pharmacol 54:73-93.
7. Bergstrom HC, Smith RF, Mollinedo NS, McDonald CG. 2010. Chronic nicotine exposure produces lateralized, age-dependent dendritic remodeling in the rodent basolateral amygdala. Synapse 64:754-764.
8. Bourgeois JP, Rakic P. 1993. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13:2801-2820.
9. Bourgeois JP, Goldman-Rakic PS, Rakic P. 1994. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4:78-96.
10. Brenhouse HC, Sonntag KC, Andersen SL. 2008. Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: Relationship to enhanced motivational salience of drug cues in adolescence. J Neurosci 28:2375-2382.
11. Casey BJ, Giedd JN, Thomas KM. 2000. Structural and functional brain development and its relation to cognitive development. Biol Psychol 54:241-257.
12. Castellano JM, Bentsen AH, Sanchez-Garrido MA, Ruiz-Pino F, Romero M, Garcia-Galiano D, Aguilar E, Pinilla L, Dieguez C, Mikkelsen JD, Tena-Sempere M. 2011. Early metabolic programming of puberty onset: Impact of changes in postnatal feeding and rearing conditions on the timing of puberty and development of the hypothalamic kisspeptin system. Endocrinology 152:3396-3408.
13. Cressman VL, Balaban J, Steinfeld S, Shemyakin A, Graham P, Parisot N, Moore H. 2010. Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat. J Comp Neurol 518:2693-2709.
14. Cunningham MG, Bhattacharyya S, Benes FM. 2002. Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. J Comp Neurol 453:116-130.
15. Cyrenne DL, Brown GR. 2011. Effects of suppressing gonadal hormones on response to novel objects in adolescent rats. Horm Behav 60:625-631.
16. Drevets WC. 1999. Prefrontal cortical-amygdalar metabolism in major depression. Ann NY Acad Sci 877:614-637.
17. Ernst M, Fudge JL. 2010. Adolescence: On the neural path to adulthood. In: Grant JE, Potenza MN, editors. Young adult mental health. New York, NY: Oxford University Press. p 19-39.
18. Ernst M, Romeo RD, Andersen SL. 2009. Neurobiology of the development of motivated behaviors in adolescence: A window into a neural systems model. Pharmacol Biochem Behav 93:199-211.
19. Giedd JN, Snell JW, Lange N, Rajapakse JC, Casey BJ, Kozuch PL, Vaituzis AC, Vauss YC, Hamburger SD, Kaysen D, Rapoport JL. 1996a. Quantitative magnetic resonance imaging of human brain development: Ages 4-18. Cereb Cortex 6:551-560.
20. Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL. 1996b. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4-18 years. J Comp Neurol 366:223-230.
21. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. 1999. Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2:861-863.
22. Glaser EM, van der Loos H. 1981. Analysis of thick brain sections by obverse-reverse computer microscopy: Application of a new, high clarity golgi-nissl stain. J Neurosci Methods 4:117-125.
23. Gould E, Woolf NJ, Butcher LL. 1991. Postnatal development of cholinergic neurons in the rat. I. forebrain. Brain Res Bull 27:767-789.
24. Graber JA, Brooks-Gunn J, Petersen AC. 1996. Transitions through adolescence: Interpersonal domains and context. Mahwah, NJ: Lawrence Erlbaum Associates.
25. Guilarte TR, 1998. The N-methyl-d-asparate receptor: Physiology and neurotoxicology in the developing brain. In: Slikker W, Jr, Chang, JL, editors. Handbook of developmental neurotoxicology. San Diego: Academic Press. p 285-304.
26. Hammerslag LR, Gulley JM. 2013. Age and sex differences in reward behavior in adolescent and adult rats. Dev Psychobiol (in press).
27. Harris KM. 1999. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol 9:343-348.
28. Heng LJ, Markham JA, Hu XT, Tseng KY. 2011. Concurrent upregulation of postsynaptic L-type Ca(2+) channel function and protein kinase A signaling is required for the periadolescent facilitation of Ca(2+) plateau potentials and dopamine D1 receptor modulation in the prefrontal cortex. Neuropharmacology 60:953-962.
29. Huttenlocher PR. 1979. Synaptic density in human frontal cortex-Developmental changes and effects of aging. Brain Res 163:195-205.
30. Huttenlocher PR, Dabholkar AS. 1997. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167-178.
31. Insel TR, Miller LP, Gelhard RE. 1990. The ontogeny of excitatory amino acid receptors in rat forebrain. I. N-methyl-d-aspartate and quisqualate receptors. Neuroscience 35:31-43.
32. Jernigan TL, Trauner DA, Hesselink JR, Tallal PA. 1991. Maturation of human cerebrum observed in vivo during adolescence. Brain 114(Pt 5):2037-2049.
33. Juraska JM. 1982. The development of pyramidal neurons after eye opening in the visual cortex of hooded rats: A quantitative study. J Comp Neurol 212:208-213.
34. Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings HB. 1988. Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol 269:58-72.
35. Kellogg CK, Taylor MK, Rodriguez-Zafra M, Pleger GL. 1993. Altered stressor-induced changes in GABAA receptor function in the cerebral cortex of adult rats exposed in utero to diazepam. Pharmacol Biochem Behav 44:267-273.
36. Kessler RC, Berglund PA, Bruce ML, Koch JR, Laska EM, Leaf PJ, Manderscheid RW, Rosenheck RA, Walters EE, Wang PS. 2001. The prevalence and correlates of untreated serious mental illness. Health Serv Res 36:987-1007.
37. Killgore WD, Oki M, Yurgelun-Todd DA. 2001. Sex-specific developmental changes in amygdala responses to affective faces. Neuroreport 12:427-433.
38. Korenbrot CC, Huhtaniemi IT, Weiner RI. 1977. Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod 17:298-303.
39. Koss WA, Franklin AD, Juraska JM. 2011. Delayed alternation in adolescent and adult male and female rats. Dev Psychobiol 53:724-731.
40. Leussis MP, Freund N, Brenhouse HC, Thompson BS, Andersen SL. 2012. Depressive-like behavior in adolescents after maternal separation: Sex differences, controllability, and GABA. Dev Neurosci 34:210-217.
41. Levin CA, Culhane KA, Hartmann J, Evankovich K, Mattson AJ, Harward H, Ringholz G, Ewing-Cobbs L, Fletcher JM. 1991. Developmental changes in performance on tests of purported frontal lobe functioning. Dev Neuropsychol 7:377-395.
42. Markham JA, Juraska JM. 2002. Aging and sex influence the anatomy of the rat anterior cingulate cortex. Neurobiol Aging 23:579-588.
43. Markham JA, Morris JR, Juraska JM. 2007. Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 144:961-968.
44. Markham JA, Mullins SE, Koenig JI. 2013. Peri-adolescent maturation of the prefrontal cortex is sex-specific and disrupted by prenatal stress. J Comp Neurol 521:1828-1843.
45. McDonald AJ. 1982. Cytoarchitecture of the central amygdaloid nucleus of the rat. J Comp Neurol 208:401-418.
46. Merke DP, Fields JD, Keil MF, Vaituzis AC, Chrousos GP, Giedd JN. 2003. Children with classic congenital adrenal hyperplasia have decreased amygdala volume: Potential prenatal and postnatal hormonal effects. J Clin Endocrinol Metab 88:1760-1765.
47. Meyer G, Ferres-Torres R, Mas M. 1978. The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study. Brain Res 155:108-112.
48. Monk CS, McClure EB, Nelson EE, Zarahn E, Bilder RM, Leibenluft E, Charney DS, Ernst M, Pine DS. 2003. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20:420-428.
49. Muller JF, Mascagni F, McDonald AJ. 2006. Pyramidal cells of the rat basolateral amygdala: Synaptology and innervation by parvalbumin-immunoreactive interneurons. J Comp Neurol 494:635-650.
50. Munoz-Cueto JA, Garcia-Segura LM, Ruiz-Marcos A. 1990. Developmental sex differences and effect of ovariectomy on the number of cortical pyramidal cell dendritic spines. Brain Res 515:64-68.
51. Murphy KM, Tcharnaia L, Beshara SP, Jones DG. 2012. Cortical development of AMPA receptor trafficking proteins. Front Mol Neurosci 5:1-12.
52. Niemi RR, Thompson WR. 1980. Pavlovian excitation, internal inhibition, and their interaction with free operant avoidance as a function of age in rats. Dev Psychobiol 13:61-76.
53. Nunez JL, Sodhi J, Juraska JM. 2002. Ovarian hormones after postnatal day 20 reduce neuron number in the rat primary visual cortex. J Neurobiol 52:312-321.
54. Primus RJ, Kellogg CK. 1991. Gonadal status and pubertal age influence the responsiveness of the benzodiazepine/GABA receptor complex to environmental challenge in male rats. Brain Res 561:299-306.
55. Rowniak M. 2013. The amygdala in the guinea pig is sexually dimorphic-A morphological study. Brain Res 1524:44-53.
56. Rubinow MJ, Juraska JM. 2009. Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: A stereological study. J Comp Neurol 512:717-725.
57. Rubinow MJ, Drogos LL, Juraska JM. 2009a. Age-related dendritic hypertrophy and sexual dimorphism in rat basolateral amygdala. Neurobiol Aging 30:137-146.
58. Rubinow MJ, Hagerbaumer DA, Juraska JM. 2009b. The food-conditioned place preference task in adolescent, adult and aged rats of both sexes. Behav Brain Res 198:263-266.
59. Schenk F. 1985. Development of place navigation in rats from weaning to puberty. Behav Neural Biol 43:69-85.
60. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, Lammers CR, Reiss AL, Amaral DG. 2004. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci 24:6392-6401.
61. Sholl DA. 1956. The measurable parameters of the cerebral cortex and their significance in its organization. Prog Neurobiol 2:324-333.
62. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW. 1999. In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859-861.
63. Spear LP. 2000. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463.
64. Tseng KY, O'Donnell P. 2005. Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cereb Cortex 15:49-57.
65. Tseng KY, O'Donnell P. 2007a. D2 dopamine receptors recruit a GABA component for their attenuation of excitatory synaptic transmission in the adult rat prefrontal cortex. Synapse 61:843-850.
66. Tseng KY, O'Donnell P. 2007b. Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb Cortex 17:1235-1240.
67. van Eden CG, Uylings HB. 1985. Postnatal volumetric development of the prefrontal cortex in the rat. J Comp Neurol 241:268-274.
68. Weinberger DR, Aloia MS, Goldberg TE, Berman KF. 1994. The frontal lobes and schizophrenia. J Neuropsychiatry Clin Neurosci 6:419-427.
69. Wiedenmayer CP. 2009. Plasticity of defensive behavior and fear in early development. Neurosci Biobehav Rev 33:432-441.
70. Yates MA, Markham JA, Anderson SE, Morris JR, Juraska JM. 2008. Regional variability in age-related loss of neurons from the primary visual cortex and medial prefrontal cortex of male and female rats. Brain Res 1218:1-12.
71. Yildirim M, Mapp OM, Janssen WG, Yin W, Morrison JH, Gore AC. 2008. Postpubertal decrease in hippocampal dendritic spines of female rats. Exp Neurol 210:339-348.
72. Zhang W, Rosenkranz JA. 2012. Repeated stress enhances basolateral amygdala neuronal activity in an age-dependent manner. Neuroscience 226:459-474.