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Original Paper

Monogamous and Promiscuous Rodent Species Exhibit Discrete Variation in the Size of the Medial Prefrontal Cortex

Kingsbury M.A.a · Gleason E.D.b · Ophir A.G.c · Phelps S.M.d · Young L.J.e · Marler C.A.b

Author affiliations

aDepartment of Biology, Indiana University, Bloomington, Ind., bDepartment of Psychology, University of Wisconsin-Madison, Madison, Wisc., cDepartment of Zoology, Oklahoma State University, Stillwater, Okla., dSection of Integrative Biology, University of Texas at Austin, Austin, Tex., and eCenter for Translational Social Neuroscience, Department of Psychiatry and Behavioral Sciences, Yerkes National Primate Research Center, Emory University, Atlanta, Ga., USA

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Brain Behav Evol 2012;80:4–14

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Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: October 31, 2011
Accepted: May 01, 2012
Published online: June 30, 2012
Issue release date: August 2012

Number of Print Pages: 11
Number of Figures: 3
Number of Tables: 1

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE

Abstract

Limbic-associated cortical areas, such as the medial prefrontal and retrosplenial cortex (mPFC and RS, respectively), are involved in the processing of emotion, motivation, and various aspects of working memory and have been implicated in mating behavior. To determine whether the independent evolution of mating systems is associated with a convergence in cortical mechanisms, we compared the size of mPFC and RS between the monogamous prairie vole (Microtus ochrogaster) and the promiscuous meadow vole (Microtus pennsylvanicus), and between the monogamous California mouse (Peromyscus californicus) and the promiscuous white-footed mouse (Peromyscus leucopus). For both promiscuous mice and voles, the mPFC occupied a significantly larger percentage of total cortex than in the monogamous species. No significant differences were observed for the RS or overall cortex size with respect to mating system, supporting the convergent evolution of mPFC size, specifically. Individual differences in the mating behavior of male prairie voles (wandering versus pair-bonding), presumably facultative tactics, were not reflected in the relative size of the mPFC, which is likely a heritable trait. Given the importance of the mPFC for complex working memory, particularly object-place and temporal order memory, we hypothesize that the relatively greater size of the mPFC in promiscuous species reflects a greater need to remember multiple individuals and the times and locations in which they have been encountered in the home range.

© 2012 S. Karger AG, Basel


References

  1. Berteaux D, Bety J, Rengifo E, Bergeron JM (1999): Multiple paternity in meadow voles (Microtus pennsylvanicus): investigating the role of the female. Behav Ecol Sociobiol 45:283–291.
  2. Boonstra R, Xia XH, Pavone L (1993): Mating system of the meadow vole, Microtus pennsylvanicus. Behav Ecol 4:83–89.
  3. Canady RA, Kroodsma DE, Nottebohm F (1984): Population differences in complexity of a learned skill are correlated with the brain space involved. Proc Natl Acad Sci USA 81:6232–6234.
  4. Carter CS, Getz LL, Cohen-Parsons M (1986): Relationships between social-organization and behavioral endocrinology in a monogamous mammal. Adv Stud Behav 16:109–145.
    External Resources
  5. Caviness VS Jr (1975): Architectonic map of neocortex of the normal mouse. J Comp Neurol 164:247–263.
  6. Clancy B, Darlington RB, Finlay BL (2001): Translating developmental time across mammalian species. Neuroscience 105:7–17.
  7. Cooper BG, Manka TF, Mizumori SJ (2001): Finding your way in the dark: the retrosplenial cortex contributes to spatial memory and navigation without visual cues. Behav Neurosci 115:1012–1028.
  8. Dalley JW, Cardinal RN, Robbins TW (2004): Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771–784.
  9. de Bruin JP, Sanchez-Santed F, Heinsbroek RP, Donker A, Postmes P (1994): A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 652:323–333.
  10. DeVries AC, Carter CS (1999): Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster). Can J Zool 77:885–889.
    External Resources
  11. DeVries AC, Devries MB, Taymans S, Carter CS (1995): Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc Natl Acad Sci USA 92:7744–7748.
  12. Dewsbury DA (1982): Dominance rank, copulatory behavior, and differential reproduction. Q Rev Biol 57:135–159.
  13. Dunbar RI, Shultz S (2007): Evolution in the social brain. Science 317:1344–1347.
  14. Finarelli JA, Flynn JJ (2009): Brain-size evolution and sociality in Carnivora. Proc Natl Acad Sci USA 106:9345–9349.
  15. Finlay BL, Darlington RB (1995): Linked regularities in the development and evolution of mammalian brains. Science 268:1578–1584.
  16. Fjallbrant TT, Manger PR, Pettigrew JD (1998): Some related aspects of platypus electroreception: temporal integration behaviour, electroreceptive thresholds and directionality of the bill acting as an antenna. Philos Trans R Soc Lond B Biol Sci 353:1211–1219.
  17. Franklin KB, Paxinos G (1997): The Mouse Brain in Stereotaxic Coordinates. San Diego, Academic Press.
  18. Gaulin SJ, FitzGerald RW (1988): Home-range size as a predictor of mating systems in Microtus. J Mammal 69:311–319.
    External Resources
  19. Gaulin SJ, FitzGerald RW (1989): Sexual selection for spatial-learning ability. Anim Behav 37:322–331.
  20. 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.
  21. Getz LL, Hofmann JE (1986): Social-organization in free-living prairie voles, Microtus ochrogaster. Behav Ecol Sociobiol 18:275–282.
  22. Gibson RM, Jewell PA (1982): Semen quality, female choice and multiple mating in domestic sheep: a test of Trivers’ sexual competence hypothesis. Behaviour 80:9–31.
    External Resources
  23. Gruder-Adams S, Getz LL (1985): Comparison of the mating system and paternal behavior in Microtus ochrogaster and Microtus pennsylvanicus. J Mammal 66:165–167.
  24. Gubernick DJ, Alberts JR (1987): The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol 101:169–177.
  25. Gundersen HJG, Jensen EB (1987): The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263.
  26. Harker KT, Whishaw IQ (2004): A reaffirmation of the retrosplenial contribution to rodent navigation: reviewing the influences of lesion, strain, and task. Neurosci Biobehav Rev 28:485–496.
    External Resources
  27. Healy SD (1991): Hippocampal volume and migration in passerine birds. Naturwissenschaften 78:242–426.
    External Resources
  28. Heske EJ, Ostfeld RS (1990): Sexual dimorphism in size, relative size of testes, and mating systems in North American voles. J Mammal 71:510–519.
    External Resources
  29. Hoover WB, Vertes RP (2007): Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149–179.
    External Resources
  30. Insel TR, Hulihan TJ (1995): A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 109:782–789.
  31. Insel TR, Preston S, Winslow JT (1995): Mating in the monogamous male: behavioral consequences. Physiol Behav 57:615–627.
  32. Insel TR, Wang ZX, Ferris CF (1994): Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14:5381–5392.
  33. Insel TR, Young LJ (2001): The neurobiology of attachment. Nat Rev Neurosci 2:129–136.
  34. Jacobs LF, Gaulin SJ, Sherry DF, Hoffman GE (1990): Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc Natl Acad Sci USA 87:6349–6352.
  35. Kaskan PM, Franco EC, Yamada ES, Silveira LC, Darlington RB, Finlay BL (2005): Peripheral variability and central constancy in mammalian visual system evolution. Proc R Soc Lond B Biol Sci 272:91–100.
  36. Kesner RP, Holbrook T (1987): Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia 25:653–664.
  37. Kesner RP, Ragozzino ME (2003): The role of the prefrontal cortex in object-place learning: a test of the attribute specificity model. Behav Brain Res 146:159–165.
    External Resources
  38. Kolb B (1990): Prefrontal cortex; in Kolb B, Tees RC (eds): The Cerebral Cortex of the Rat. Cambridge, MIT Press, pp 437–458.
  39. Kolb B, Tees RC (1990): The Cerebral Cortex of the Rat. Cambridge, MIT Press.
  40. Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL (1989): Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 86:1388–1392.
  41. Krubitzer L, Kaas J (2005): The evolution of the neocortex in mammals: how is phenotypic diversity generated? Curr Opin Neurobiol 15:444–453.
  42. Leingartner A, Thuret S, Kroll TT, Chou SJ, Leasure JL, Gage FH, O’Leary DD (2007): Cortical area size dictates performance at modality-specific behaviors. Proc Natl Acad Sci USA 104:4153–4158.
    External Resources
  43. MacLean EL, Barrickman NL, Johnson EM, Wall CE (2009): Sociality, ecology, and relative brain size in lemurs. J Hum Evol 56:471–478.
    External Resources
  44. Madison DM (1980a): Space use and social structure in meadow voles, Microtus pennsylvanicus. Behav Ecol Sociobiol 7:65–71.
    External Resources
  45. Madison DM (1980b): An integrated view of the social biology of Microtus pennsylvanicus. Biologist 62:20–33.
  46. McBride WJ, Murphy JM, Ikemoto S (1999): Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav Brain Res 101:129–152.
  47. Mcguire B, Novak M (1984): A comparison of maternal-behavior in the meadow vole (Microtus pennsylvanicus), prairie vole (Microtus ochrogaster) and pine vole (Microtus pinetorum). Anim Behav 32:1132–1141.
  48. Michalczyk L, Millard AL, Martin OY, Lumley AJ, Emerson BC, Chapman T, Gage MJ (2011): Inbreeding promotes female promiscuity. Science 333:1739–1742.
  49. Nottebohm F (1981): A brain for all seasons: cyclical anatomical changes in song control. Science 214:1368–1370.
  50. Oliveras D, Novak M (1986): A comparison of paternal behavior in the meadow vole Microtus pennsylvanicus, the pine vole Microtus pinetorum and the prairie vole Microtus ochrogaster. Anim Behav 34:519–526.
  51. Ophir AG, Gessel A, Zheng DJ, Phelps SM (2012): Oxytocin receptor density is associated with male mating tactics and social monogamy. Horm Behav 61:445–453.
  52. Ophir AG, Wolff JO, Phelps SM (2008): Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc Natl Acad Sci USA 105:1249–1254.
  53. Ostfeld RS, Pugh SR, Seamon JO, Tamarin RH (1988): Space use and reproductive success in a population of meadow voles. J Anim Ecol 57:385–394.
  54. Parker GA (1970): Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567.
    External Resources
  55. Paxinos G, Watson C (1998): The rat brain in stereotaxic coordinates, ed 4. San Diego, Academic Press.
  56. Pitnick S, Jones KE, Wilkinson GS (2006): Mating system and brain size in bats. Proc R Soc Lond B Biol Sci 273:719–724.
  57. Pollen AA, Dobberfuhl AP, Scace J, Igulu MM, Renn SC, Shumway CA, Hofmann HA (2007): Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav Evol 70:21–39.
  58. Ragozzino ME, Detrick S, Kesner RP (1999a): Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19:4585–4594.
  59. Ragozzino ME, Wilcox C, Raso M, Kesner RP (1999b): Involvement of rodent prefrontal cortex subregions in strategy switching. Behav Neurosci 113:32–41.
  60. Ribble DO (1991): The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:161–166.
  61. Ribble DO, Salvioni M (1990): Social-organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent. Behav Ecol Sociobiol 26:9–15.
  62. Roth TC 2nd, Ladage LD, Freas CA, Pravosudov VV (2012): Variation in memory and the hippocampus across populations from different climates: a common garden approach. Proc R Soc Lond B Biol Sci 279:402–410.
    External Resources
  63. Roth TC, Pravosudov VV (2009): Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc R Soc Lond B Biol Sci 276:401–405.
  64. Safi K, Dechmann DK (2005): Adaptation of brain regions to habitat complexity: a comparative analysis in bats (chiroptera). Proc R Soc Lond B Biol Sci 272:179–186.
  65. Sakai ST, Arsznov BM, Lundrigan BL, Holekamp KE (2011): Brain size and social complexity: a computed tomography study in hyaenidae. Brain Behav Evol 77:91–104.
  66. Shapiro LE, Dewsbury DA (1990): Differences in affiliative behavior, pair bonding, and vaginal cytology in 2 species of vole (Microtus ochrogaster and Microtus montanus). J Comp Psychol 104:268–274.
  67. Shapiro LE, Leonard CM, Sessions CE, Dewsbury DA, Insel TR (1991): Comparative neuroanatomy of the sexually dimorphic hypothalamus in monogamous and polygamous voles. Brain Res 541:232–240.
  68. Sherry DF, Forbes MR, Khurgel M, Ivy GO (1993): Females have a larger hippocampus than males in the brood-parasitic brown-headed cowbird. Proc Natl Acad Sci USA 90:7839–7843.
  69. Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989): The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317.
  70. Shultz S, Dunbar RI (2006): Both social and ecological factors predict ungulate brain size. Proc R Soc Lond B Biol Sci 273:207–215.
  71. Shultz S, Dunbar RI (2007): The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc R Soc Lond B Biol Sci 274:2429–2436.
  72. Smeltzer MD, Curtis JT, Aragona BJ, Wang Z (2006): Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci Lett 394:146–151.
  73. Stockley P, Searle JB, Macdonald DW, Jones CS (1993): Female multiple mating-behavior in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B Biol Sci 254:173–179.
  74. Thornhill R, Alcock J (1983): The Evolution of Insect Mating Systems. Cambridge, Harvard University Press.
  75. Vann SD, Aggleton JP, Maguire EA (2009): What does the retrosplenial cortex do? Nat Rev Neurosci 10:792–802.
  76. Wang Z, Liu Y, Young LJ, Insel TR (1997a): Developmental changes in forebrain vasopressin receptor binding in prairie voles (Microtus ochrogaster) and montane voles (Microtus montanus). Ann NY Acad Sci 807:510–513.
  77. Wang Z, Young LJ, Liu Y, Insel TR (1997b): Species differences in vasopressin receptor binding are evident early in development: comparative anatomic studies in prairie and montane voles. J Comp Neurol 378:535–546.
  78. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993): A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548.
  79. Wolff JO (1985a): Behaviour; in Tamarin RH (ed): Biology of New World Microtus. Spec Publ Soc Mammal 8:340–372.
  80. Wolff JO (1985b): The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can J Zool 63:2657–2662.
    External Resources
  81. Xia XH, Millar JS (1988): Paternal behavior by Peromyscus leucopus in enclosures. Can J Zool 66:1184–1187.
    External Resources
  82. Xia XH, Millar JS (1989): Dispersion of adult male Peromyscus leucopus in relation to female reproductive status. Can J Zool 67:1047–1052.
    External Resources
  83. Xia XH, Millar JS (1991): Genetic-evidence of promiscuity in Peromyscus leucopus. Behav Ecol Sociobiol 28:171–178.
  84. Young LJ, Lim MM, Gingrich B, Insel TR (2001): Cellular mechanisms of social attachment. Horm Behav 40:133–138.
  85. Young LJ, Wang Z (2004): The neurobiology of pair bonding. Nat Neurosci 7:1048–1054.
  86. Yunger JA (2004): Movement and spatial organization of small mammals following vertebrate predator exclusion. Oecologia 139:647–654.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: October 31, 2011
Accepted: May 01, 2012
Published online: June 30, 2012
Issue release date: August 2012

Number of Print Pages: 11
Number of Figures: 3
Number of Tables: 1

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE


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