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Hippocampus and Spatial Memory in Brood Parasitic Cowbirds

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Avian Brood Parasitism

Part of the book series: Fascinating Life Sciences ((FLS))

Abstract

Natural selection can modify cognition and its neural mechanisms if these modifications enhance fitness. Brood parasites are ideal subjects to study sex-specific adaptations in cognition and the brain because it is often females that search for potential host nests, and some species as a result show a reversal of sex-typical space use usually seen in mammals. Research from North and South America shows that female brown-headed (Molothrus ater) and shiny (M. bonariensis) cowbirds have a larger hippocampus than males, and female brown-headed cowbirds exhibit more hippocampal neurogenesis than males. Female cowbirds have better spatial memory than males in some tasks, especially tasks requiring long-term spatial memory in an ecologically relevant context. The hippocampus and spatial memory in cowbirds appear to be specialized for brood parasitism. Because of their diversity and unusual breeding biology, brood parasites offer many opportunities for investigating general questions about the adaptive modification of cognition and the brain.

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References

  • Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, Hsiang HLL, Wheeler AL, Guskjolen A, Niibori Y, Shoji H, Ohira K, Richards BA, Miyakawa T, Josselyn SA, Frankland PW (2014) Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344:598–602

    Article  CAS  Google Scholar 

  • Astié AA, Kacelnik A, Reboreda JC (1998) Sexual differences in memory in shiny cowbirds. Anim Cogn 1:77–82

    Article  PubMed  Google Scholar 

  • Astié AA, Scardamaglia RC, Muzio RN, Reboreda JC (2015) Sex differences in retention after a visual or a spatial discrimination learning task in brood parasitic shiny cowbirds. Behav Process 119:99–104

    Article  Google Scholar 

  • Balthazart J, Ball GF (2014a) Doublecortin is a highly valuable endogenous marker of adult neurogenesis in canaries. Commentary on Vellema M et al (2014): Evaluating the predictive value of doublecortin as a marker for adult neurogenesis in canaries (Serinus canaria). Journal of Comparative Neurology 522, 1299–1315. Brain Behav Evol 84:1–4

    Article  PubMed  PubMed Central  Google Scholar 

  • Balthazart J, Ball GF (2014b) Endogenous versus exogenous markers of neurogenesis in canaries and other birds: advantages and disadvantages. J Comp Neurol 522:4100–4120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burger DK, Gulbrandsen T, Saucier DM, Iwaniuk AN (2014) The effects of season and sex on dentate gyrus size and neurogenesis in a wild rodent, Richardson’s ground squirrel (Urocitellus richardsonii). Neuroscience 272:240–251

    Article  CAS  PubMed  Google Scholar 

  • Burns JG, Foucaud J, Mery F (2011) Costs of memory: lessons from ‘mini’ brains. Proc R Soc B Biol Sci 278:923–929

    Article  Google Scholar 

  • Clayton NS, Reboreda JC, Kacelnik A (1997) Seasonal changes of hippocampus volume in parasitic cowbirds. Behav Process 41:237–243

    Article  CAS  Google Scholar 

  • Cole EF, Morand-Ferron J, Hinks AE, Quinn JL (2012) Cognitive ability influences reproductive life history variation in the wild. Curr Biol 22:1808–1812

    Article  CAS  PubMed  Google Scholar 

  • Epp JR, Mera RS, Köhler S, Josselyn SA, Frankland PW (2016) Neurogenesis-mediated forgetting minimizes proactive interference. Nat Commun 7:10838

    Google Scholar 

  • Fraga RM (1986) The bay-winged cowbirds (Molothrus badius) and it brood parasites: interactions, coevolution and comparative efficiency. Ph. D. dissertation, University of California, Santa Barbara

    Google Scholar 

  • Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, McConnell SK (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23(2):247–256

    Article  CAS  PubMed  Google Scholar 

  • Fusani L, Van’t Hof T, Hutchison JB, Gahr M (2000) Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J Neurobiol 43:254–268

    Article  CAS  PubMed  Google Scholar 

  • Galea LA, Kavaliers M, Ossenkopp KP (1996) Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol 199:195–200

    PubMed  CAS  Google Scholar 

  • Garland T, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828

    Article  Google Scholar 

  • Gates JE, Evans DR (1998) Cowbirds breeding in the central Appalachians: spatial and temporal patterns and habitat selection. Ecol Appl 8:27–40

    Article  Google Scholar 

  • Gaulin SJ, FitzGerald RW (1986) Sex differences in spatial ability: an evolutionary hypothesis and test. Am Nat 127:74–88

    Article  Google Scholar 

  • Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257–271

    Article  CAS  PubMed  Google Scholar 

  • Gloag R, Fiorini VD, Reboreda JC, Kacelnik A (2013) The wages of violence: mobbing by mockingbirds as a frontline defence against brood-parasitic cowbirds. Anim Behav 86:1023–1029

    Article  Google Scholar 

  • Gloag R, Fiorini VD, Reboreda JC, Kacelnik A (2014) Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests. Behav Ecol Sociobiol 68:681–689

    Article  Google Scholar 

  • Guigueno MF, Snow DA, MacDougall-Shackleton SA, Sherry DF (2014) Female cowbirds have more accurate spatial memory than males. Biol Lett 10:20140026

    Article  PubMed  PubMed Central  Google Scholar 

  • Guigueno MF, MacDougall-Shackleton SA, Sherry DF (2015) Sex differences in spatial memory in brown-headed cowbirds: males outperform females on a touchscreen task. PloS One 10(6):e0128302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guigueno MF, MacDougall-Shackleton SA, Sherry DF (2016) Sex and seasonal differences in hippocampal volume and neurogenesis in brood-parasitic brown-headed cowbirds (Molothrus ater). Dev Neurobiol 76:1275–1290

    Article  PubMed  Google Scholar 

  • Hasenstaub A, Otte S, Callaway E, Sejnowski TJ (2010) Metabolic cost as a unifying principle governing neuronal biophysics. Proc Natl Acad Sci U S A 107:12329–12334

    Article  PubMed  PubMed Central  Google Scholar 

  • Hodgson ZG, Meddle SL, Christians JK, Sperry TS, Healy SD (2008) Influence of sex steroid hormones on spatial memory in a songbird. J Comp Physiol A 194:963–969

    Article  CAS  Google Scholar 

  • Huston JP, Hasenöhrl RU (1995) The role of neuropeptides in learning: focus on the neurokinin substance P. Behav Brain Res 66:117–127

    Article  CAS  PubMed  Google Scholar 

  • Johnson KP, Lanyon SM (1999) Molecular systematics of the grackles and allies, and the effect of additional sequence (cyt b and ND2). Auk 116:759–768

    Article  Google Scholar 

  • Lanyon SM, Omland KE (1999) A molecular phylogeny of the blackbirds (Icteridae): five lineages revealed by cytochrome-b sequence data. Auk 116:629–639

    Article  Google Scholar 

  • Lowther PE (1993) Brown-headed cowbird (Molothrus ater). In: Poole A (ed) The birds of North America Online. Cornell Lab of Ornithology, Ithaca. Retrieved from the Birds of North America Online http://bna.birds.cornell.edu.proxy2.lib.uwo.ca/bna/species/047

  • Mason P (1987) Pair formation in cowbirds: evidence found for screaming but not shiny cowbirds. Condor:349–356

    Google Scholar 

  • Metzdorf R, Gahr M, Fusani L (1999) Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol 407:115–129

    Article  CAS  PubMed  Google Scholar 

  • Moser EI, Kropff E, Moser M-B (2008) Pace cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31:69–89

    Article  CAS  PubMed  Google Scholar 

  • Murphy DD, Segal M (1996) Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 16:4059–4068

    Article  CAS  PubMed  Google Scholar 

  • Nairne JS, Pandeirada JN (2008) Adaptive memory: remembering with a stone-age brain. Curr Dir Psychol Sci 17:239–243

    Article  Google Scholar 

  • Nair-Roberts RG, Erichsen JT, Reboreda JC, Kacelnik A (2006) Distribution of substance P reveals a novel subdivision in the hippocampus of parasitic South American cowbirds. J Comp Neurol 496:610–626

    Article  CAS  PubMed  Google Scholar 

  • O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428

    Article  PubMed  Google Scholar 

  • Postma A, Jager G, Kessels RP, Koppeschaar HP, van Honk J (2004) Sex differences for selective forms of spatial memory. Brain Cogn 54:24–34

    Article  PubMed  Google Scholar 

  • Pravosudov VV, Roth TCI (2013) Cognitive ecology of food hoarding: the evolution of spatial memory and the hippocampus. Annu Rev Ecol Syst 44:173–193

    Article  Google Scholar 

  • Reboreda JC, Clayton NS, Kacelnik A (1996) Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport 7:505–508

    Article  CAS  PubMed  Google Scholar 

  • Roth TC, Pravosudov VV (2009) Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc R Soc B Biol Sci 276:401–405

    Article  Google Scholar 

  • Rothstein SI, Yokel DA, Fleischer RC (1986) Social dominance, mating and spacing systems, female fecundity, and vocal dialects in captive and free-ranging brown-headed cowbirds. In: Johnston RF (ed) Current ornithology. Plenum, New York, pp 127–185

    Chapter  Google Scholar 

  • Saldanha CJ, Popper P, Micevych PE, Schlinger BA (1998) The passerine hippocampus is a site of high aromatase: inter-and intraspecies comparisons. Horm Behav 34:85–97

    Article  CAS  PubMed  Google Scholar 

  • Scardamaglia RC, Reboreda JC (2014) Ranging behavior of female and male shiny cowbirds and Screaming Cowbirds while searching for host nests. Auk 131:610–618

    Article  Google Scholar 

  • Scardamaglia RC, Fiorini VD, Kacelnik A, Reboreda JC (2017) Planning host exploitation through prospecting visits by parasitic cowbirds. Behav Ecol Sociobiol 71:23

    Article  Google Scholar 

  • Sealy SG (1992) Removal of yellow warbler eggs in association with cowbird parasitism. Condor 94:40–54

    Article  Google Scholar 

  • Shen P, Campagnoni CW, Kampf K, Schlinger BA, Arnold AP, Campagnoni AT (1994) Isolation and characterization of a zebra finch aromatase cDNA: in situ hybridization reveals high aromatase expression in brain. Mol Brain Res 24:227–237

    Article  CAS  PubMed  Google Scholar 

  • Sherry DF (2006) Neuroecology. Annu Rev Psychol 57:167–197

    Article  PubMed  Google Scholar 

  • Sherry DF, Schacter DL (1987) The evolution of multiple memory systems. Psychol Rev 94(4):439

    Article  Google Scholar 

  • Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317

    Article  CAS  PubMed  Google Scholar 

  • Sherry DF, Jacobs LF, Gaulin SJ (1992) Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:298–303

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 90:7839–7843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverman I, Choi J, Mackewn A, Fisher M, Moro J, Olshansky E (2000) Evolved mechanisms underlying wayfinding: further studies on the hunter-gatherer theory of spatial sex differences. Evol Hum Behav 21:201–213

    Article  CAS  PubMed  Google Scholar 

  • Smulders TV (2006) A multi-disciplinary approach to understanding hippocampal function in food-hoarding birds. Rev Neurosci 17:53–69

    Article  PubMed  Google Scholar 

  • Strausberger BM, Ashley MV (2003) Breeding biology of brood parasitic brown-headed cowbirds (Molothrus ater) characterized by parent-offspring and sibling-group reconstruction. Auk 120(2):433–445

    Article  Google Scholar 

  • Vellema M, Hertel M, Urbanus SL, Linden A, Gahr M (2014) Evaluating the predictive value of doublecortin as a marker for adult neurogenesis in canaries (Serinus canaria). J Comp Neurol 522(6):1299–1315

    Article  CAS  PubMed  Google Scholar 

  • White DJ, Ho L, Freed-Brown G (2009) Counting chicks before they hatch: female cowbirds can time readiness of a host nest for parasitism. Psychol Sci 20:1140–1145

    Article  PubMed  Google Scholar 

  • Williams CL, Barnett AM, Meck WH (1990) Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104:84–97

    Article  CAS  PubMed  Google Scholar 

  • Woolfenden BE, Gibbs LH, Sealy SG (2002) High opportunity for sexual selection in both sexes of an obligate brood parasitic bird, the brown-headed cowbird (Molothrus ater). Behav Ecol Sociobiol 52(5):417–425

    Article  Google Scholar 

  • Woolley CS, McEwen BS (1994) Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680–7687

    Article  CAS  PubMed  Google Scholar 

  • Yankova M, Hart SA, Woolley CS (2001) Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc Natl Acad Sci U S A 98:3525–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the reviewers, Juan C. Reboreda, Romina C. Scardamaglia, and Manolo Soler, for constructive comments on earlier drafts of this chapter.

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Correspondence to Mélanie F. Guigueno .

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Guigueno, M.F., Sherry, D.F. (2017). Hippocampus and Spatial Memory in Brood Parasitic Cowbirds. In: Soler, M. (eds) Avian Brood Parasitism. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-73138-4_11

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