No effect of social group composition or size on hippocampal formation morphology and neurogenesis in mountain chickadees (Poecile gambeli)
Corresponding Author
Rebecca A. Fox
Department of Biology, University of Nevada, Reno, Nevada
Department of Biology, University of Nevada, Reno, NevadaSearch for more papers by this authorTimothy C. Roth II
Department of Biology, University of Nevada, Reno, Nevada
Search for more papers by this authorLara D. LaDage
Department of Biology, University of Nevada, Reno, Nevada
Search for more papers by this authorVladimir V. Pravosudov
Department of Biology, University of Nevada, Reno, Nevada
Search for more papers by this authorCorresponding Author
Rebecca A. Fox
Department of Biology, University of Nevada, Reno, Nevada
Department of Biology, University of Nevada, Reno, NevadaSearch for more papers by this authorTimothy C. Roth II
Department of Biology, University of Nevada, Reno, Nevada
Search for more papers by this authorLara D. LaDage
Department of Biology, University of Nevada, Reno, Nevada
Search for more papers by this authorVladimir V. Pravosudov
Department of Biology, University of Nevada, Reno, Nevada
Search for more papers by this authorAbstract
Brain plasticity and adult neurogenesis may play a role in many ecologically important processes including mate recognition, song learning and production, and spatial memory processing. In a number of species, both physical and social environments appear to influence attributes (e.g., volume, neuron number, and neurogenesis) of particular brain regions. The hippocampus in particular is well known to be especially sensitive to such changes. Although social grouping in many taxa includes the formation of male and female pairs, most studies of the relationship between social environment and the hippocampus have typically considered only solitary animals and those living in same-sex groups. Thus, the aim of this study was to compare the volume of the hippocampal formation, the total number of hippocampal neurons, and the number of immature neurons in the hippocampus (as determined by doublecortin expression) in mountain chickadees (Poecile gambeli) housed in groups of males and females, male–female pairs, same sex pairs of either males or females, and as solitary individuals. The different groups were visually and physically, but not acoustically, isolated from each other. We found no significant differences between any of our groups in hippocampal volume, the total number of hippocampal neurons, or the number of immature neurons. Our results thus provided no support to the hypothesis that social group composition and/or size have an effect on hippocampal morphology and neurogenesis. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70:538–547, 2010
REFERENCES
- Balthazart J,Boseret G,Konkle ATM,Hurley LL,Ball GF. 2008. Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC. Eur J Neurosci 27: 801–817.
- Barnea A,Mishal A,Nottebohm F. 2006. Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: An anatomical representation of time? Behav Brain Res 167: 63–74.
- Barnea A,Nottebohm F. 1994. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91: 11217–11221.
- Baudoin C,Busquet N,Dobson FS,Gheusi G,Feron C,Durand J-L,Heth G, et al. 2005. Male-female associations and female olfactory neurogenesis with pair bonding in Mus spicilegus. Biol J Linn Soc 84: 323–334.
- Brown JP,Couillard-Després S,Cooper-Kuhn CM,Winkler J,Aigner L,Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467: 1–10.
- Couillard-Després S,Winner B,Schaubeck S,Aigner R,Vroemen M,Weidner N,Bogdahn U, et al. 2005. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21: 1–14.
- Drapeu E,Mayo W,Arousseu C,Le Moal M,Piazza PV,Abrous DN. 2003. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Nat Acad Sci USA 100: 14385–14390.
- Ekman J. 1989. Ecology of non-breeding social systems of Parus. Wilson Bull 101: 263–288.
- Emery NJ,Seed AM,von Bayern AMP,Clayton NS. 2007. Cognitive adaptations of social bonding in birds. Philos Trans R Soc B 362: 489–505.
- Eriksson PS,Perfilieva E,Bjork-Eriksson T,Alborn AM,Nordberg C,Peterson DA,Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313–1317.
- Faul F,Erfelder E,Buchner A,Lang A-G. 2007. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 41: 1149–1160.
- Fowler C,Liu Y,Ouimet C,Wang Z. 2002. The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51: 115–128.
- Garcia-Verdugo JM,Ferron S,Flames N,Collado L,Desfilis E,Font E. 2002. The proliferative ventricular zone in adult vertebrates: A comparative study using reptiles, birds, and mammals. Brain Res Bull 57: 765–775.
- Gould E,Beylin A,Tanapat P,Reeves A,Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2: 260–265.
- Griffiths R,Double MC,Orr K,Dawson RJG. 1998. A DNA test to sex most birds. Mol Ecol 7: 1071–1075.
- Gundersen HJG,Jensen EB. 1987. The efficiency of systematic sampling in stereology and its predictions. J Microsc Oxford 147: 229–263.
- Hairston IS,Little MTM,Scanlon MD,Barakat MT,Palmer TD,Sapolsky RM,Heller HC. 2005. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J Neurophysiol 94: 4224–4233.
- Hawken PAR,de St. Jorre JJ,Rodger J,Esmaili T,Blache D,Martin GB. 2009. Rapid induction of cell proliferation in the adult female ungulate brain (Ovis aries) associated with activation of the reproductive axis by exposure to unfamiliar males. Biol Reprod 80: 1146–1151.
- Ibi D,Takuma K,Koike H,Mizoguchi H,Tsuritani K,Kuwahara Y,Kamei H, et al. 2008. Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J Neurochem 3: 921–932.
- Jacobs BL,van Praag H,Gage FH. 2000. Adult brain neurogenesis and psychiatry: A novel theory of depression. Mol Psychiatry 5: 262–269.
- Kempermann G. 2002. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22: 635–638.
- Kempermann G,Kuhn HG,Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493–495.
- Kempermann G,Wiskott L,Gage FH. 2004. Functional significance of adult neurogenesis. Curr Opin Neurobiol 14: 186–191.
- Kikusui T,Winslow JT,Mori Y. 2006. Social buffering: Relief from stress and anxiety. Philos Trans R Soc B 361: 2215–2228.
- Kozorovitskiy Y,Gould E. 2004. Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J Neurosci 24: 6755–6759.
- Krebs JR,Sherry DF,Healy SD,Perry VH,Vaccarino AL. 1989. Hippocampal specialization of food-storing birds. Proc Nat Acad Sci USA 86: 1388–1392.
- LaDage LD,Roth TC,Fox RA,Pravosudov VV. 2009. Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees. Behav Neurosci 123: 284–291.
- LaDage LD,Roth TC,Fox RA,Pravosudov VV. 2010. Ecologically-relevant spatial memory use modulates hippocampal neurogenesis. Proc R Soc B 277: 1071–1079.
- Leasure JL,Decker L. 2009. Social isolation prevents exercise-induced proliferation of hippocampal progenitor cells in female rats. Hippocampus 19: 907–912.
- Lemmon D,Withiam ML,Barkan CPL. 1997. Mate protection and winter pair-bonds in black-capped chickadees. Condor 99: 424–433.
- Lipkind D,Nottebohm F,Rado R,Barnea A. 2002. Social change affects the survival of new neurons in the forebrain of adult songbirds. Behav Brain Res 133: 31–43.
- Lu L,Bao B,Chen H,Xia P,Fan X,Zhang J,Pei G, et al. 2003. Modification of hippocampal neurogenesis and neuroplasticity by social environments. Exp Neurol 183: 600–609.
- Mak GK,Enwere EK,Gregg C,Pakarainen T,Poutanen M,Huhtaniemi I,Weiss S. 2007. Male pheromone-stimulated neurogenesis in the adult female brain: Possible role in mating behavior. Nat Neurosci 10: 1003–1011.
- Malberg JE,Schechter LE. 2005. Increasing hippocampal neurogenesis: A novel mechanism for antidepressant drugs. Curr Pharm Des 11: 145–155.
- McEwen BS. 1999. Stress and hippocampal plasticity. Ann Rev Neurosci 22: 105–122.
- McEwen BS. 2007. Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 87: 873–904.
- Nacher J,Alonso-Llosa G,Rosell DR,McEwen BS. 2002. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging 24: 273–284.
- Nottebohm F. 2002. Why are some neurons replaced in adult brain? J Neurosci 22: 624–628.
- Nottebohm F. 2005. The neural basis of birdsong. PLOS Biol 3: e164.
- Pravosudov VV,Clayton NS. 2002. A test of the adaptive specialization hypothesis: Population differences in caching, memory and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav Neurosci 116: 515–522.
- Pravosudov VV,Lavenex P,Clayton NS. 2002. Changes in spatial memory mediated by experimental variation in food supply do not affect hippocampal anatomy in mountain chickadees (Poecile gambeli). J Neurobiol 51: 142–148.
- Pravosudov VV,Lavenex P,Omanska A. 2005. Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. Behav Neurosci 119: 1368–1374.
- Pravosudov VV,Mendoza SP,Clayton NS. 2003. The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli). Horm Behav 44: 93–102.
- Pravosudov VV,Omanska A. 2005. Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees. J Neurobiol 62: 31–41.
- Rao MS,Shetty AK. 2004. Efficacy of doublecortin as a marker to analyze the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19: 234–246.
- Roth TC,Pravosudov VV. 2009. Hippocampal volume and neuron numbers increase along a gradient of environmental harshness: A large-scale comparison. Proc R Soc B 276: 401–405.
- Rukstalis M,French JA. 2005. Vocal buffering of the stress response: Exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Horm Behav 47: 1–7.
- Sapolsky RM. 2004. Why Zebras Don't Get Ulcers. New York: Henry Holt. 564 p.
- SAS Institute, Inc. 2008. SAS 9.2 User's Guide. Cary, NC: SAS Institute, Inc.
- Smith MT,Pencea V,Wang Z,Luskin MB,Insel TR. 2001. Increased number of BrdU-labeled neurons in the rostral migratory stream of the estrous prairie vole. Horm Behav 39: 11–21.
- Smulders TV,Sasson AD,DeVoogd TJ. 1995. Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J Neurobiol 27: 15–25.
- Smulders TV,Shiflett MW,Sperling AJ,DeVoogd TJ. 2000. Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: The black-capped chickadee. J Neurobiol 44: 414–422.
- Sørensen C,Øverli Ø,Summers CH,Nilsson G. 2007. Social regulation of neurogenesis in teleosts. Brain Behav Evol 70: 239–246.
- Stranahan AM,Khali D,Gould E. 2006. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9: 526–533.
- Takeda K-I,Sato S,Sugawara K. 2003. Familiarity and group size affect emotional stress in Japanese black heifers. Appl Anim Behav Sci 82: 1–11.
- Tramontin AD,Wingfield JC,Brenowitz EA. 1999. Contributions of social cues and photoperiod to seasonal plasticity in the adult avian song control system. J Neurosci 19: 476–483.
- van Praag H,Christie BR,Sejnowski TJ,Gage FH. 1999a. Running enhances neurogenesis, learning and long-term potentiation in mice. Proc Nat Acad Sci USA 96: 13427–13431.
- van Praag H,Kempermann G,Gage FH. 1999b. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266–270.
- van Praag H,Kempermann G,Gage FH. 2000. Neural consequences of environmental enrichment. Nat Rev Neurosci 1: 191–198.
- Veenema AH,de Kloet ER,de Wilde MC,Roelofs AJ,Kawata M,Buwalda B,Neumann ID, et al. 2007. Differential effects of stress on adult hippocampal cell proliferation in low and high aggressive mice. J Neuroendocrinol 19: 489–498.
- West MJ,Slomianka L,Gundersen HJG. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482–497.