The avian hippocampus and the hypothetical maps used by navigating migratory birds (with some reflection on compasses and migratory restlessness)

Barkan S, Yom-Tov Y, Barnea A (2014) A possible relation between new neuronal recruitment and migratory behavior in Acrocephalus warblers. Dev Neurobiol 74(12):1194–1209 Barkan S, Roll U, Yom-Tov Y, Wassenaar, LI, Barnea A (2016) Possible linkage between neuronal recruitment and flight distance in migratory birds. Sci R 6:21983 Bartell PA, Gwinner E (2005) A separate circadian oscillator controls nocturnal migratory restlessness in the songbird Sylvia borin. J Biol Rhythms 20:538–549 Bingman VP, Able KP (2002) Maps in birds: representational mechanisms and neural bases. Curr Opin Neurobiol 12:745–750 Bingman VP, Cheng K (2005) Mechanisms of animal global navigation: comparative perspectives and enduring challenges. Ethol Ecol Evol 17:295–318 Bingman VP, Jones TJ (1994) Sun compass based spatial learning impaired in homing pigeons with hippocampal lesions. J Neurosci 14:6687–6694 Bingman VP, Sharp PE (2006) Neuronal implementation of hippocampal-mediated spatial behavior: a comparative evolutionary perspective. Behav Cogn Neurosci Rev 5(2):80–91 Bingman VP, Bagnoli P, Ioalé P, Casini G (1984) Homing behavior of pigeons after telencephalic ablations. Brain Behav Evolut 24:94–106 Bingman VP, Gagliardo A, Ioalé P (1996) Hippocampal participation in the sun compass orientation of phase-shifted homing pigeons. J Comp Physiol A 179:695–702 Bingman VP, Able KP, Siegel JJ (1999) Hippocampal lesions do not impair the geomagnetic orientation of migratory Savannah sparrows. J Comp Physiol A 185:577–581 Bingman VP, Gagliardo A, Hough II GE, Ioalè P, Kahn MC, Siegel JJ (2005) The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integr Comp Biol 45:555–564. Bingman VP, Rodríguez F, Salas C (2017) The hippocampus and non-mammalian vertebrates. In: Kaas J (ed) Evolution of nervous systems, 2nd edn. Academic Press, pp 479–489 Budzynski CA, Gagliardo A, Ioalé P, Bingman VP (2002) Participation of the homing pigeon thalamofugal visual pathway in sun-compass associative learning. Eur J Neurosci 15(1):197–210 Cassone VM (2014) Avian circadian organization: a chorus of clocks. Front Neuroendocrinol 35(1):76–88 Cristol DA, Reynolds EB, Leclerc JE, Donner AH, Farabaugh CS, Ziegenfus CW (2003) Migratory dark-eyed juncos, Junco hyemalis, have better spatial memory and denser hippocampal neurons than nonmigratory conspecifics. Anim Behav 66:317–328 Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16:366–381 Deutschlander ME, Phillips JB, Munro U (2012) Age-dependent orientation to magnetically-simulated geographic displacements in migratory Australian silvereyes (Zosterops l. lateralis). Wilson J Ornithol 124(3):467–477 Diniz CG, Magalhães NGM, Sousa AA, Santos Filho C, Diniz DG, Lima CM, Picanço-Diniz CW (2016) Microglia and neurons in the hippocampus of migratory sandpipers. Braz J Med Biol Res 49(1):1–10 Eichenbaum H, Cohen NJ (2014) Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83(4):764–770 Fuchs R, Bingman VP, Ross JD, Bernroider G (2015) Brain contrasts between migratory and nonmigratory North American lark sparrows (Chondestes grammacus). NeuroReport 26(17):1011–1016 Fusani L, Cardinale M, Schwabl I, Goymann W (2011) Food availability but not melatonin affects nocturnal restlessness in a wild migrating passerine. Horm Behav 59(1):187–192 Gagliardo A (2013) Forty years of olfactory navigation in birds. J Exp Biol 216(12):2165–2171 Gagliardo A, Ioalé P, Bingman VP (1999) Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. J Neuro 19:311–315 Gagliardo A, Ioalè P, Savini M, Lipp HP, Dell’Omo G (2007) Finding home: the final step of the pigeons’ homing process studied with a GPS data logger. J Exp Biol 210(7):1132–1138 Gagliardo A, Ioalè P, Savini M, Dell’Omo G, Bingman VP (2009) Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Eur J Neurosci 29:2389–2400 Gagliardo A, Bried J, Lambardi P, Luschi P, Wilkelski M, Bonadonna F (2013) Oceanic navigation in Cory’s shearwaters: evidence for a crucial role of olfactory cues for homing after displacement. J Exp Biol 216(15):2798–2805 Gagliardo A, Pollonara E, Coppola VJ, Santos CD, Wikelski M, Bingman VP (2014) Evidence for perceptual neglect of environmental features in hippocampal-lesioned pigeons during homing. Eur J Neurosci 40(7):3102–3110 Giocomo LM, Stensola T, Bonnevie T, Van Cauter T, Moser MB, Moser EI (2014) Topography of head direction cells in medial entorhinal cortex. Curr Biol 24(3):252–262 Guilford T, Åkesson S, Gagliardo A, Holland RA, Mouritsen H, Muheim R, Bingman VP (2011) Migratory navigation in birds: new opportunities in an era of fast-developing tracking technology. J Exp Biol 214(22):3705–3712 Gwinner E (1986) Circannual rhythms. Springer, Berlin Hahn TP, Brazeal KR, Schultz EM, Chmura HE, Cornelius JM, Watts HE, MacDougall-Shackleton SA (2014) Annual schedules. In: Scanes C (ed) Sturkie’s avian physiology, 6th edn. Academic Press, Cambridge, pp 847–867 Healy SD, Gwinner E, Krebs JR (1996) Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav Brain Res 81:61–68 Healy SD, Bacon IE, Haggis O, Harris AP, Kelley LA (2009) Explanations for variation in cognitive ability: behavioural ecology meets comparative cognition. Behav Process 80:288–294 Heinze S, Reppert SM (2011) Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69(2):345–358 Herold C, Coppola VJ, Bingman VP (2015) The maturation of research into the avian hippocampal formation: recent discoveries from one of nature’s foremost navigators. Hippocampus 25:1193–1211 Holland RA, Thorup K, Gagliardo A, Bisson IA, Knecht E, Mizrahi D, Wikelski M (2009) Testing the role of sensory systems in the migratory heading of a songbird. J Exp Biol 212(24):4065–4071 Ikegami K, Yoshimura T (2012) Circadian clocks and the measurement of daylength in seasonal reproduction. Mol Cell Endocrinol 349(1):76–81 Ioalé P, Gagliardo A, Bingman VP (2000a) Hippocampal participation in navigational map learning in young homing pigeons is dependent on training experience. Eur J Neurosci 12:742–750 Ioalé P, Gagliardo A, Bingman VP (2000b) Further experiments on the relationship between hippocampus and orientation following phase-shift in homing pigeons. Behav Brain Res 108(2):157–167 Juss TS, Meddle SL, Servant RS, King VM (1993) Melatonin and photoperiodic time measurement in Japanese quail (Coturnix coturnix japonica). Proc R Soc Lond B Biol Sci 254:21–28 Keary N, Bischof HJ (2012) Activation changes in zebra finch (Taeniopygia guttata) brain areas evoked by alterations of the earth magnetic field. PloS One 7(6):1–8 Ketterson ED, Nolan V Jr (1990) Site attachment and site fidelity in migratory birds: experimental evidence from the field and analogies from neurobiology. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 117–129 Kishkinev D, Chernetsov N, Pakhomov A, Heyers D, Mouritsen H (2015) Eurasian reed warblers compensate for virtual magnetic displacement. Curr Biol 25(19):822–824 Kishkinev D, Heyers D, Woodworth BK, Mitchell GW, Hobson KA, Norris DR (2016) Experienced migratory songbirds do not display goal-orientation after release following a cross-continental displacement: an automated telemetry study. Sci Rep 6:37326 Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser MB (2008) Finite scale of spatial representation in the hippocampus. Science 321:140–143 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 Kuenzel WJ (1974) Multiple effects of ventromedial hypothalamic lesions in the white-throated sparrow, Zonotrichia albicollis. J Comp Physiol 90(2):169–182 Kuenzel WJ, Helms CW (1970) Hyperphagia, polydipsia, and other effects of hypothalamic lesions in the White-throated Sparrow, Zonotrichia albicollis. Condor 72(1):66–75 Kumar V (2010) Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol Biochem Zool 83:827–835 McMillan JP (1972) Pinealectomy abolishes the rhythm of migratory restlessness. J Comp Physiol 79:105–112 Mouritsen H, Heyers D, Güntürkün O (2016) The neural basis of long-distance navigation in birds. Annu Rev Physiol 78:133–154 Németh Z, Luo Y, Owen JC, Moore FR (2016) Seasonal variation in CREB expression in the hippocampal formation of first year migratory songbirds: implications for the role of memory during migration. The Auk 134(1):146–152 O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford Pollonara E, Luschi P, Guilford T, Wikelski M, Bonadonna F, Gagliardo A (2015) Olfaction and topography, but not magnetic cues, control navigation in a pelagic seabird: displacements with shearwaters in the Mediterranean Sea. Sci Rep 5:1–10 Pravosudov VV, Kitaysky AS, Omanska A (2006) The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison. Proc Biol Sci 273:2641–2649 Ralph C J (1978) Disorientation and possible fate of young passerine coastal migrants. Bird Banding 49(3):237–247 Rastogi A, Kumari Y, Rani S, Kumar V (2013) Neural correlates of migration: activation of hypothalamic clock (s) in and out of migratory state in the blackheaded bunting (Emberiza melanocephala). PloS One 8(10):e70065 Safi K, Gagliardo A, Wikelski M, Kranstauber B (2016) How displaced migratory birds could use volatile atmospheric compounds to find their migratory corridor? A test using a particle dispersion model. Front Behav Neurosci 10:1–9 Schiller D, Eichenbaum H, Buffalo EA, Davachi L, Foster DJ, Leutgeb S, Ranganath C (2015) Memory and space: towards an understanding of the cognitive map. J Neuro 35(41):13904–13911 Sherry DF (2006) Neuroecology. Annu Rev Psychol 57:167–197 Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317 Siegel JJ, Nitz D, Bingman VP (2006) Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons. Hippocampus 16(2):125–140 Striedter GF (2016) Evolution of the hippocampus in reptiles and birds. J Comp Neurol 524(3):496–517 Taube JS, Muller RU, Ranck JB (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10(2):420–435 Thorup K, Bisson IA, Bowlin MS, Holland RA, Wingfield JC, Ramenofsky M, Wikelski M (2007) Evidence for a navigational map stretching across the continental US in a migratory songbird. Proc Natl Acad Sci 104(46):18115–18119 Thorup K, Tøttrup AP, Willemoes M, Klaassen RHG, Strandberg R, Vega ML, Dasari HP, Araújo MB, Wikelski M, Rahbek C (2017) Resource tracking within and across continents in long-distance migrants. Sci Adv 3:e1601360 Trivedi AK, Malik S, Rani S, Kumar V (2016) Pinealectomy abolishes circadian behavior and interferes with circadian clock gene oscillations in brain and liver but not retina in a migratory songbird. Physiol Behav 156:156–163 Vargas JP, Siegel JJ, Bingman VP (2006) The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus. Brain Res Bull 70(2):158–164 Wallraff HG (2005) Avian navigation: pigeon homing as a paradigm. Springer, Berlin Wallraff HG, Neumann MF (1989) Contribution of olfactory navigation and non-olfactory pilotage to pigeon homing. Behav Ecol Sociobiol 25:293–302 Wang G, Ramenofsky M, Wingfield JC (2013) Apparent dissociation of photoperiodic time measurement between vernal migration and breeding under dim green light conditions in Gambel’s white-crowned sparrows Zonotrichia leucophrys bambelii. Curr Zool 59:349–359. Wikelski M, Arriero E, Gagliardo A, Holland RA, Huttunen MJ, Juvaste R, Alanko M (2015) True navigation in migrating gulls requires intact olfactory nerves. Sci Rep 5:1–11 Wiltschko R, Wiltschko W (2003) Avian navigation: from historical to modern concepts. Anim Behav 65(2):257–272 Wiltschko R, Schiffner I, Fuhrmann P, Wiltschko W (2010) The role of the magnetite-based receptors in the beak in pigeon homing. Curr Biol 20(17):1534–1538 Wu LQ, Dickman JD (2011) Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr Biol 21(5):418–423 Yokoyama K (1976) Hypothalamic and hormonal control of the photoperiodically induced vernal functions in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Cell Tissue Res 174(3):391–416 Zapka M, Heyers D, Hein CM, Engels S, Schneider NL, Hans J, Weiler S, Dreyer D, Kishkinev K, Wild JM, Mouritsen H (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461(7268):1274–1277 Zúñiga D, Falconer J, Fudickar AM, Jensen W, Schmidt A, Wikelski M, Partecke J (2016) Abrupt switch to migratory night flight in a wild migratory songbird. Sci Rep 6:34207