Individual differences in cortical connections of somatosensory cortex are associated with parental rearing style in prairie voles (Microtus ochrogaster)

Journal of Comparative Neurology

Volumn 524, Issue 3, 2016, Pages 564-577

  Seelke, Adele M H ^a   Perkeybile, Allison M ^a,b   Grunewald, Rebecca ^a   Bales, Karen L ^a   Krubitzer, Leah A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Development; Epigenetics; Individual differences; Primary somatosensory cortex; S1

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CHILD REARING; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; FRONTAL CORTEX; MALE; MICROTUS OCHROGASTER; NONHUMAN; PARIETAL CORTEX; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; PROGENY; STIMULUS RESPONSE; TACTILE STIMULATION; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL BEHAVIOR; ARVICOLINAE; COMPARATIVE STUDY; HEMISPHERIC DOMINANCE; MATERNAL BEHAVIOR; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; PATERNAL BEHAVIOR; PSYCHOLOGY; SOMATOSENSORY CORTEX; TOUCH;

ANIMALS; ARVICOLINAE; BEHAVIOR, ANIMAL; FEMALE; FUNCTIONAL LATERALITY; MALE; MATERNAL BEHAVIOR; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; PATERNAL BEHAVIOR; SOMATOSENSORY CORTEX; TOUCH; TOUCH PERCEPTION;

EID: 84953637210     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23837     Document Type: Article

References (51)

1. Adams DL, Horton JC. 2003. Capricious expression of cortical columns in the primate brain. Nat Neurosci 6:113-114.
2. Bales KL, Carter CS. 2003. Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178-184.
3. Bales KL, van Westerhuyzen JA, Lewis-Reese AD, Grotte ND, Lanter JA, Carter CS. 2007. Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles. Horm Behav 52:274-279.
4. Bales KL, Perkeybile AM, Conley OG, Lee MH, Guoynes CD, Downing GM, Yun CR, Solomon M, Jacob S, Mendoza SP. 2013. Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles. Biol Psychiatry 74:180-188.
5. Bishop KM, Rubenstein JL, O'Leary DD. 2002. Distinct actions of Emx1, Emx2, and Pax6 in regulating the specification of areas in the developing neocortex. J Neurosci 22:7627-7638.
6. Campi KL, Karlen SJ, Bales KL, Krubitzer L. 2007. Organization of sensory neocortex in prairie voles (Microtus ochrogaster). J Comp Neurol 502:414-426.
7. Campi KL, Bales KL, Grunewald R, Krubitzer L. 2010. Connections of auditory and visual cortex in the prairie vole (Microtus ochrogaster): evidence for multisensory processing in primary sensory areas. Cereb Cortex 20:89-108.
8. Champagne FA. 2008. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386-397.
9. Champagne FA, Curley JP. 2009. Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci Biobehav Rev 33:593-600.
10. Champagne FA, Francis DD, Mar A, Meaney MJ. 2003. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79:359-371.
11. Chang EF, Merzenich MM. 2003. Environmental noise retards auditory cortical development. Science 300:498-502.
12. Chapman B. 2000. Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287:2479-2482.
13. Chapman B, Jacobson MD, Reiter HO, Stryker MP. 1986. Ocular dominance shift in kitten visual cortex caused by imbalance in retinal electrical activity. Nature 324:154-156.
14. Chittka A. 2010. Dynamic distribution of histone H4 arginine 3 methylation marks in the developing murine cortex. PloS One 5:e13807.
15. Cho B, Kim HJ, Kim H, Sun W. 2011. Changes in the histone acetylation patterns during the development of the nervous system. Exp Neurobiol 20:81-84.
16. Cooke DF, Padberg J, Zahner T, Krubitzer L. 2012. The functional organization and cortical connections of motor cortex in squirrels. Cereb Cortex 22:1959-1978.
17. Dooley JC, Franca JG, Seelke AMH, Cooke DF, Krubitzer LA. 2013. A connection to the past: Monodelphis domestica provides insight into the organization and connectivity of the brains of early mammals. J Comp Neurol 521:3877-3897.
18. Fox K. 1994. The cortical component of experience-dependent synaptic plasticity in the rat barrel cortex. J Neurosci 14:7665-7679.
19. Francis D, Diorio J, Liu D, Meaney MJ. 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155-1158.
20. Francis DD, Champagne FC, Meaney MJ. 2000. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145-1148.
21. Fuentes P, Canovas J, Berndt FA, Noctor SC, Kukuljan M. 2012. CoREST/LSD1 control the development of pyramidal cortical neurons. Cereb Cortex 22:1431-1441.
22. Getz LL, Carter CS, Gavish L. 1981. The mating system of the prairie vole, Microtus-ochrogaster: field and laboratory evidence for pair bonding. Behav Ecol Sociobiol 8:189-194.
23. Goldberg AD, Allis CD, Bernstein E. 2007. Epigenetics: a landscape takes shape. Cell 128:635-638.
24. Golshani P, Hutnick L, Schweizer F, Fan G. 2005. Conditional Dnmt1 deletion in dorsal forebrain disrupts development of somatosensory barrel cortex and thalamocortical long-term potentiation. Thalamus Rel Syst 3:227-233.
25. Hackman DA, Farah MJ, Meaney MJ. 2010. Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat Rev Neurosci 11:651-659.
26. Hamasaki T, Leingartner A, Ringstedt T, O'Leary DD. 2004. EMX2 regulates sizes and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors. Neuron 43:359-372.
27. Hammock EA, Young LJ. 2002. Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour. Eur J Neurosci 16:399-402.
28. Harlow HF, Zimmermann RR. 1959. Affectional responses in the infant monkey; orphaned baby monkeys develop a strong and persistent attachment to inanimate surrogate mothers. Science 130:421-432.
29. Jain N, Catania KC, Kaas JH. 1998. A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations. Cereb Cortex 8:227-236.
30. Jain N, Qi HX, Catania KC, Kaas JH. 2001. Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys. J Comp Neurol 429:455-468.
31. Karlen SJ, Krubitzer L. 2006. Phenotypic diversity is the cornerstone of evolution: variation in cortical field size within short-tailed opossums. J Comp Neurol 499:990-999.
32. Kenkel WM, Suboc G, Carter CS. 2014. Autonomic, behavioral, and neuroendocrine correlates of paternal behavior in male prairie voles. Physiol Behav 128:252-259.
33. Krubitzer L, Dooley JC. 2013. Cortical plasticity within and across lifetimes: how can development inform us about phenotypic transformations? Front Hum Neurosci 7:620.
34. Krubitzer LA, Seelke AMH. 2012. Cortical evolution in mammals: the bane and beauty of phenotypic variability. Proc Natl Acad Sci U S A 109(Suppl 1):10647-10654.
35. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ. 2000a. Maternal care, hippocampal synaptogenesis, and cognitive development in rats. Nat Neurosci 3:799-806.
36. Macri S, Laviola G, Leussis MP, Andersen SL. 2010. Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats. Psychoneuroendocrinology 35:392-402.
37. Nott A, Nitarska J, Veenvliet JV, Schacke S, Derijck AA, Sirko P, Muchardt C, Pasterkamp RJ, Smidt MP, Riccio A. 2013. S-nitrosylation of HDAC2 regulates the expression of the chromatin-remodeling factor Brm during radial neuron migration. Proc Natl Acad Sci U S A 110:3113-3118.
38. O'Leary DD, Sahara S. 2008. Genetic regulation of arealization of the neocortex. Curr Opin Neurobiol 18:90-100.
39. Perkeybile AM, Griffin LL, Bales KL. 2013. Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster). Front Behav Neurosci 7:21.
40. Perkeybile AM, Delaney-Busch N, Hartman S, Grimm KJ, Bales KL. 2015. Intergenerational transmission of alloparenting and oxytocin and vasopressing receptor distribution. Front Behav Neurosci In press. Frontiers in Behavioral Neuroscience.
41. 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 69:663-673.
42. Rash BG, Grove EA. 2006. Area and layer patterning in the developing cerebral cortex. Curr Opin Neurobiol 16:25-34.
43. Seelke AMH, Padberg J, Disbrow E, Purnell S, Recanzone G, Krubitzer L. 2011. Topographic maps within Brodmann's area 5 of macaque monkeys. Cereb Cortex 22:1834-1850.
44. Seelke AMH, Dooley JC, Krubitzer LA. 2012. The emergence of somatotopic maps of the body in s1 in rats: the correspondence between functional and anatomical organization. PloS One 7:e32322.
45. Shepherd GM, Pologruto TA, Svoboda K. 2003. Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277-289.
46. Smit-Rigter LA, Champagne DL, van Hooft JA. 2009. Lifelong impact of variations in maternal care on dendritic structure and function of cortical layer 2/3 pyramidal neurons in rat offspring. PloS One 4:e5167.
47. Tagawa Y, Kanold PO, Majdan M, Shatz CJ. 2005. Multiple periods of functional ocular dominance plasticity in mouse visual cortex. Nat Neurosci 8:380-388.
48. Takatsuru Y, Yoshitomo M, Nemoto T, Eto K, Nabekura J. 2009. Maternal separation decreases the stability of mushroom spines in adult mice somatosensory cortex. Brain Res 1294:45-51.
49. Tennant KA, Adkins DL, Donlan NA, Asay AL, Thomas N, Kleim JA, Jones TA. 2011. The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb Cortex 21:865-876.
50. Thomas JA, Birney EC. 1979. Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav Ecol Sociobiol 5:171-186.
51. Williams JR, Catania KC, Carter CS. 1992. Development of partner preferences in female prairie voles (Microtus ochrogaster)-the role of social and sexual experience. Horm Behav 26:339-349.