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Original Paper

Sex and the Frontal Cortex: A Developmental CT Study in the Spotted Hyena

Arsznov B.M.a · Lundrigan B.L.b · Holekamp K.E.b · Sakai S.T.a, c

Author affiliations

Departments of aPsychology, bZoology and Michigan State University Museum, and cNeuroscience Program, Michigan State University, East Lansing, Mich., USA

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Brain Behav Evol 2010;76:185–197

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Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: April 23, 2010
Accepted: September 13, 2010
Published online: November 17, 2010
Issue release date: January 2011

Number of Print Pages: 13
Number of Figures: 6
Number of Tables: 0

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

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

Abstract

The purpose of this study was to examine developmental and individual variation in total endocranial volume and regional brain volumes, including the anterior cerebrum, posterior cerebrum and cerebellum/brain stem, in the spotted hyena (Crocuta crocuta). The spotted hyena is a highly gregarious animal noted for living in large, hierarchically organized groups. The social lives of male and female spotted hyenas do not differ until after puberty, when males disperse from the natal group, while females remain philopatric. Here we sought to determine whether the divergent life histories of male and female spotted hyenas are linked to differences in brain size or organization. Three-dimensional virtual endocasts were created using computed tomography from 46 spotted hyenas skulls (23 females, 22 males, 1 unknown sex) ranging in age from 1 day to 18 years. Brain volume and skull length were highly correlated (r = 0.91), and both reached asymptotic values by 34 months of age. Analyses of total endocranial volume (relative to skull length) and cerebellum/brain stem volume (relative to total endocranial volume) revealed no sex differences. However, relative anterior cerebrum volume, comprised mainly of frontal cortex, was significantly greater in adult males than adult females, and relative posterior cerebrum volume was greater in adult females than adult males. We hypothesize that the demands of neural processing underlying enhanced social cognition required for successful male transfer between matriarchical social groups at dispersal may be greater than cognitive demands on philopatric females.

© 2010 S. Karger AG, Basel


References

  1. Adolphs R (2001): The neurobiology of social cognition. Curr Opinion Neurobiol 11:231–239.
  2. Allen JS, Damasio H, Grabowski TJ (2002): Normal neuroanatomical variation in the human brain: An MRI-volumetric study. Am J Phys Ant 118:341–358.
  3. Amodio DM, Frith CD (2006): Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268–277.
  4. Boydston EE, Kapheim KM, Van Horn RC, Smale L, Holekamp KE (2005): Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyaena (Crocuta crocuta). J Zool 267:271–281.
    External Resources
  5. Breedlove SM (1994): Sexual differentiation of the human nervous system. Ann Rev Psych 45:389–429.
  6. Brutkowski S (1965): Functions of Prefrontal Cortex in Animals. Physiol Rev 45:721.
  7. Brutkowski S, Dabrowska J (1963): Disinhibition after Prefrontal Lesions as a Function of Duration of Intertrial Intervals. Science 139:505–506.
  8. Bufkin JL, Luttrell VR (2005): Neuroimaging Studies of Aggressive and Violent Behavior. Trauma, Violence and Abuse 6:176–191.
  9. Bush EC, Allman JM (2004): The scaling of frontal cortex in primates and carnivores. Proc Natl Acad Sci 101:3962–3966.
  10. DeCarli C, Massaro J, Harvey D, Hald J, Tullberg M, Auf R, Beiser A, D’Agostino R, Wolf PA (2005): Measures of brain morphology and infarction in the framingham heart study: establishing what is normal. Neurobiol Aging 26:491–510.
  11. Drea CM, Frank LG (2003): The social complexity of spotted hyenas; in De Waal FBM, Tyack PL (eds): Animal Social Complexity. Cambridge, Mass., Harvard University Press, pp 121–148.
  12. Dunbar RIM (1998): The social brain hypothesis. Evol Anthro 6:178–190.
    External Resources
  13. East ML, Hofer H (2001): Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behav Ecol 12:558–568.
  14. Ellis L, Herschberger S, Field E, Wersinger S, Pellis S, Geary D, Palmer C, Hoyenga K, Hetsroni A, Karadi K (2008): Sex Differences: Summarizing More Than a Century of Scientific Research. New York, Psychology Press.
  15. Engh AL, Esch K, Smale L, Holekamp KE (2000): Mechanisms of maternal rank ‘inheritance’ in the spotted hyena, Crocuta crocuta. Anim Behav 60:323–332.
  16. Falk D, Froese N, Sade DS, Dudek BG (1999): Sex differences in brain/body relationships of Rhesus monkeys and humans. J Human Evol 36:233–238.
  17. Frank LG (1986): Social organization of the spotted hyaena (Crocuta crocuta): II. Dominance and reproduction. Anim Behav 35:1510–1527.
    External Resources
  18. Frank LG, Glickman SE, Powch I (1990): Sexual dimorphism in the spotted hyena (Crocuta crocuta). J Zool 221:308–313.
    External Resources
  19. Fuster JM (2002): Frontal lobe and cognitive development. J Neurocytol 31:373–385.
  20. Glickman SE, Frank LG, Pavgi S (1992): Hormonal correlates of masculinization in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity. J. Reproduction and Fertility 95:451–462.
  21. Glickman SE, Frank LG, Holekamp KE, Smale L, Licht P (1993): Costs and benefits of ‘androgenization’ in the female spotted hyena: the natural selection of physiological mechanisms; in Bateson PPG (ed): Perspectives in Ethology, vol. 10, Behavior and Evolution. New York, Plenum Press, pp 87–117.
  22. Glickman SE, Short RV, Renfree MB (2005): Sexual differentiation in three unconventional mammals: Spotted hyenas, elephants and tammar wallabies. Horm Behav 48:403–417.
  23. Goldstein JM, Seidman LG, Horton NJ, Mikris N, Kennedy DN, Caviness VS, Faraone SV, Tsuang MT (2001): Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebr Cortex 11:490–497.
  24. Gorska T (1974): Functional organization of cortical motor areas in adult dogs and puppies. Acta Neurobiol Exp 34:171–203.
  25. Gur RC, Gunning-Dixon F, Bilker WB, Gur RE (2002): Sex differences in temporo-limbic and frontal brain volumes in healthy adults. Cerebr Cortex 12:998–1003.
  26. Hamilton WJ, Tilson RL, Frank LG (1986): Sexual monomorphism in spotted hyenas, Crocuta crocuta. Ethology 71:63–73.
    External Resources
  27. Hardin WB Jr, Arumugasamy N, Jameson HD (1968): Pattern of localization in ‘precentral’ motor cortex of raccoon. Brain Res 11:611–617.
  28. Hassler R, Muhs-Clement K (1964): Architectonic construction of the sensomotor and parietal cortex in the cat. J. Hirnforsch 20:377–420.
  29. Henschel JR, Skinner JD (1987): Social relationships and dispersal patterns in a clan of spotted hyaenas (Crocuta crocuta) in the Kruger National Park. S Afr J Zool 22:18–24.
  30. Holekamp KE, Smale L (1998): Dispersal status influences hormones and behavior in the male spotted hyena. Horm Behav 33:205–216.
  31. Holekamp KE, Smale L, Szykman M (1996): Rank and reproduction in the female spotted hyaena. J Reprod Fert 108:229–237.
  32. Holekamp KE, Cooper SM, Katona CI, Berry NA, Frank LG, Smale L (1997): Patterns of Association among Female Spotted Hyenas (Crocuta crocuta). J Mammalogy 78:55–64.
  33. Holekamp KE, Sakai ST, Lundrigan BL (2007): Social intelligence in the spotted hyena (Crocuta crocuta). Philosophic Trans R Soc London B 362:523–528.
  34. Holekamp KE, Smale L (1993): Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with other immature individuals. Anim Behav 46:451–466.
  35. Iversen SD, Mishkin M (1970): Preservative interference in monkeys following selective lesions of inferior prefrontal convexity. Exp Brain Res 11:376.
  36. Janis CM (1990): Correlation of cranial and dental variables with body size in ungulates and macropodoids; in Damuth J, MacFadden BJ (eds): Body Size in Mammalian Paleobiology, Estimations and Biological Implications. Cambridge, Cambridge University, Press, pp 255–300.
  37. Jerison HJ (1973): Evolution of the brain and intelligence. London: Academic Press.
  38. Jerison HJ (2007): What fossils tell us about the evolution of the neocortex; in Kaas JH, Krubitzer LA (eds): Evolution of Nervous System. New York and Oxford, Elsevier.
  39. Kawamura J (1971): Variations of the cerebral sulci in the cat. Acta Anat 80:204–221.
  40. Kruuk H (1972): The spotted hyena: a study of predation and social behavior. Chicago: University of Chicago Press.
  41. Lenroot RK, Giedd JN (2006): Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neuro Biobehav Rev 30:718–729.
  42. Leonard CM, Towler S, Welcome S, Halderman LK, Otto R, Eckert MA, Chiarello C (2008): Size Matters: Cerebral Volume Influences Sex Differences in Neuroanatomy. Cerebr Cortex 18:2920–2931.
  43. Macrini TE, Rowe T, Vandeberg JL (2007): Cranial endocasts from a growth series of Monodelphis domestica (Didelphidae, Marsupialia): a study of individual and ontogenetic variation. J Morphol 268:844.
  44. Malkova L, Heuer E, Saunders RC (2006): Longitudinal magnetic resonance imaging study of rhesus monkey brain development. Eur J Neurosci 24:3204–3212.
  45. Mills MGL (1990): Kalahari hyenas: the behavioural ecology of two species. Unwin Hyman, London.
  46. Mishkin M (1964): Perseveration of central sets after frontal lesions in monkeys; in Warren JM, Akert K (eds): The Frontal Granular Cortex and Behavior. New York, McGraw-Hill, pp 219–241.
  47. Myasnikov AA, Dykes, RW, Leclerc, SS (1997): Correlating cytoarchitecture and function in cat primary somatosensory cortex: The challenge of individual differences. Brain Res 750:95–108.
  48. Nopoulos P, Flaum M, O’Leary D, Andreasen NC (2000): Sexual dimorphism in the human brain: evaluation of tissue volume, tissue composition and surface anatomy using magnetic resonance imaging. Psychiatry Res: Neuroimaging Section 98:1–13.
  49. Pakkenberg B, Gundersen (1997): Neocortical neuron number in humans: Effect of sex and age. J Comp Neurol 384:312–320.
  50. Radinsky LB (1969): Outlines of canid and felid brain evolution. Ann NY Acad Sci 167:277–288.
    External Resources
  51. Rodrigues C (1991): Anatomical differences involving the archicortex and the neocortex of male and female brains: A quantitative study of 20 brains of each sex. Hum Evol 6:451–459.
    External Resources
  52. Sakai ST (1982): The thalamic connectivity of the primary motor cortex (MI) in the raccoon. J Comp Neurol 204:238–252.
  53. Sakai ST (1990): Corticospinal projections from area-4 and area-6 in the raccoon. Exp Brain Res 79:240–248.
  54. Sakai ST, Stanton GB, Isaacson LG (1993): Thalamic afferents of area 4 and 6 in the dog: a multiple retrograde fluorescent dye study. Anat Embry 188:551–559.
  55. Smale L, Nunes S, Holekamp KE (1997): Sexually dimorphic dispersal in mammals: Patterns, causes, and consequences; in Slater PJB, Rosenblatt J, Snowden CT, Milinski M (eds): Advances in the Study of Behavior, vol 26. San Diego, Academic Press, pp 181–250.
  56. Stanton GB, Tanaka D, Sakai ST, Weeks OI (1986): Thalamic afferents to cytoarchitectonic subdivisions of area 6 on the anterior sigmoid gyrus of the dog: a retrograde and anterograde tracing study. J Comp Neurol 252:446–467.
  57. Szykman M, Engh AL, Van Horn R C, Funk S, Scribner KT, Holekamp KE (2001): Association patterns between male and female spotted hyenas reflect male mate choice. Behav Ecol Sociobiology 50:231–238.
  58. Szykman M, Engh AL, Van Horn RC, Scribner KT, Smale Holekamp KE (2003): Rare male aggression directed toward females in a female-dominated society: baiting behavior in the spotted hyena. Aggressive Beh 29:457–474.
  59. Tanaka D (1987): Neostriatal projections from cytoarchitectonically defined gyri in the prefrontal cortex of the dog. J Comp Neurol 261:48–73.
  60. Tanner JB, Smale L, Holekamp KE (2007): Ontogenetic variation in the play behavior of spotted hyenas (Crocuta crocuta). J Devel Processes 2:5–30.
  61. Tanner JB, Zelditch ML, Lundrigan BL, Holekamp KE (2009): Ontogenetic change in skull morphology and mechanical advantage in the spotted hyena (Crocuta crocuta). J Morphol 271:353–365.
    External Resources
  62. Taylor AB, van Schaik CP (2007): Variation in brain size and ecology in Pongo. J Human Evol 52:59–71.
  63. Tilson RT, Hamilton WJ (1984): Social dominance and feeding patterns of spotted hyaenas. Anim Behav 32:715–724.
  64. Van Horn RC, Engh A, Scribner KT, Funk SM, Holekamp KE (2004): Behavioral structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Mol Ecol 13:449–458.
  65. Van Valkenburgh BV (1990). Skeletal and dental predictors of body mass in carnivores; in Damuth J, MacFadden BJ (eds): Body Size in Mammalian Paleobiology, Estimations and Biological Implications. Cambridge, Cambridge University Press, pp 181–206.
  66. Watts HE, Tanner JB, Lundrigan BL, Holekamp KE (2009): Postweaning maternal effects and the evolution of female dominance in the spotted hyena. Proc R Soc Lond B 276:2291–2298.
  67. Welker WI, Seidenstein S (1959): Somatic sensory representation in the cerebral cortex of the raccoon (Procyon lotor). J Comp Neurol 111:469–501.
  68. Wood JL, Heitmiller D, Andreasen NC, Nopoulos P (2008): Morphology of the Ventral Frontal Cortex: Relationship to Femininity and Social Cognition. Cerebr Cortex 18:534–540.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: April 23, 2010
Accepted: September 13, 2010
Published online: November 17, 2010
Issue release date: January 2011

Number of Print Pages: 13
Number of Figures: 6
Number of Tables: 0

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

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


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