Network structure of functional hippocampal lateralization in birds

Hippocampus

Volumn 25, Issue 11, 2015, Pages 1418-1428

  Jonckers, Elisabeth ^a   Güntürkün, Onur ^b   De Groof, Geert ^a   Van der Linden, Annemie ^a   Bingman, Verner P ^c  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c BOWLING GREEN STATE UNIVERSITY   (United States)

Author keywords

Functional connectivity; Hemispheric dominance; Resting state fMRI

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; BIRD; BRAIN ASYMMETRY; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; LEFT HEMISPHERE; MALE; NEUROIMAGING; NONHUMAN; PIGEON; PRIORITY JOURNAL; RIGHT HEMISPHERE; ANIMAL; BRAIN MAPPING; HEMISPHERIC DOMINANCE; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PIGEONS AND DOVES; PSYCHOLOGY; STARLING;

ANIMALS; BIRDS; BRAIN MAPPING; COLUMBIDAE; FEMALE; FUNCTIONAL LATERALITY; HIPPOCAMPUS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; STARLINGS;

EID: 84946490632     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22462     Document Type: Article

References (68)

1. Abellan A, Desfilis E, Medina L. 2014. Combinatorial expression of lef1, lhx2, lhx5, lhx9, lmo3, lmo4, and prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. Front Neuroanat 8:59.
2. Adam R, Gunturkun O. 2009. When one hemisphere takes control: Metacontrol in pigeons (columba livia). PLoS One 4:e5307.
3. Babiloni C, Carducci F, Del Gratta C, Demartin M, Romani GL, Babiloni F, Rossini PM. 2003. Hemispherical asymmetry in human SMA during voluntary simple unilateral movements. An fMRI study. Cortex 39:293-305.
4. Belcheva I, Tashev R, Belcheva S. 2007. Hippocampal asymmetry in serotonergic modulation of learning and memory in rats. Laterality 12:475-486.
5. Bingman VP, Siegel JJ, Gagliardo A, Erichsen JT. 2006. Representing the richness of avian spatial cognition: Properties of a lateralized homing pigeon hippocampus. Rev Neurosci 17:17-28.
6. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
7. Clayton N. 1993. Lateralization and unilateral transfer of spatial memory in marsh-tits. J comp Physiol A 171:807-815.
8. Clayton NS, Krebs JR. 1994. Hippocampal growth and attrition in birds affected by experience. Proc Natl Acad Sci U S A 91:7410-7414.
9. DeGroof G, Jonckers E, Gunturkun O, Denolf P, Van Auderkerke J, Van der Linden A. 2013. Functional MRI and functional connectivity of the visual system of awake pigeons. Beh Brain Res 239:43-50.
10. Folta K, Diekamp B, Gunturkun O. 2004. Asymmetrical modes of visual bottom-up and top-down integration in the thalamic nucleus rotundus of pigeons. J Neurosci 24:9475-9485.
11. Freeman HD, Cantalupo C, Hopkins WD. 2004. Asymmetries in the hippocampus and amygdala of chimpanzees (pan troglodytes). Behav Neurosci 118:1460-1465.
12. Gagliardo A, Ioale P, Odetti F, Bingman VP, Siegel JJ, Vallortigara G. 2001. Hippocampus and homing in pigeons: Left and right hemispheric differences in navigational map learning. Eur J Neurosci 13:1617-1624.
13. Gagliardo A, Vallortigara G, Nardi D, Bingman VP. 2005. A lateralized avian hippocampus: Preferential role of the left hippocampal formation in homing pigeon sun compass-based spatial learning. Eur J Neurosci 22:2549-2559.
14. Gao Z, Goldstein A, Harpaz Y, Hansel M, Zion-Golumbic E, Bentin S. 2013. A magnetoencephalographic study of face processing: M170, gamma-band oscillations and source localization. Hum Brain Mapp 34:1783-1795.
15. Grandjean J, Schroeter A, Batata I, Rudin M (2014) Optimization of anesthesia protocol for resting-state fMRI in mice based on differential effects of anesthetics on functional connectivity patterns. Neuroimage 102;838-847.
16. Gunturkun O. 1997. Avian visual lateralization: A review. Neuroreport 8:iii-xi.
17. Gunturkun O, Hellmann B, Melsbach G, Prior H. 1998. Asymmetries of representation in the visual system of pigeons. Neuroreport 9:4127-4130.
18. Gunturkun O, Verhoye M, De GG, Van Der Linden A. 2013. A 3-dimensional digital atlas of the ascending sensory and the descending motor systems in the pigeon brain. Brain Struct Funct 218; 269-281.
19. Harris KD, Csicsvari J, Hirase H, Dragoi G, Buzsaki G. 2003. Organization of cell assemblies in the hippocampus. Nature 424:552-556.
20. Hauk O, Davis MH, Ford M, Pulvermuller F, Marslen-Wilson WD. 2006. The time course of visual word recogni.ion as revealed by linear regression analysis of ERP data. Neuroimage 30:1383-1400.
21. Hauk O, Coutout C, Holden A, Chen Y. 2012. The time-course of single-word reading: Evidence from fast behavioral and brain responses. Neuroimage 60:1462-1477.
22. Hein CM, Engels S, Kishkinev D, Mouritsen H. 2011. Robins have a magnetic compass in both eyes. Nature 471:E11-E12; discussion E12-E13.
23. Herold C, Bingman VP, Strockens F, Letzner S, Sauvage M, Palomero-Gallagher N, Zilles K, Gunturkun O. 2014. Distribution of neurotransmitter receptors and zinc in the pigeon (columba livia) hippocampal formation: A basis for further comparison with the mammalian hippocampus. J Comp Neurol 522:2553-2575.
24. Ivanova M, Ternianov A, Belcheva S, Tashev R, Negrev N, Belcheva I. 2008. Hippocampal asymmetry in exploratory behavior to vasoactive intestinal polypeptide. Peptides 29:940-947.
25. Jonckers E, Van Audekerke J, De Visscher G, Van der Linden A, Verhoye M. 2011. Functional connectivity FMRI of the rodent brain: Comparison of functional connectivity networks in rat and mouse. PLoSOne 6:e18876-
26. Jonckers E, Delgado Y Palacios R, Shah D, Guglielmetti C, Verhoye M, Van der Linden A. 2014. Different anesthesia regimes modulate the functional connectivity outcome in mice. Magn Reson Med 72;1103-1112.
27. Kalthoff D, Seehafer JU, Po C, Wiedermann D, Hoehn M. 2011. Functional connectivity in the rat at 11.7T: Impact of physiological noise in resting state fMRI. Neuroimage 54;2828-2839.
28. Kawakami R, Shinohara Y, Kato Y, Sugiyama H, Shigemoto R, Ito I. 2003. Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science 300:990-994.
29. Klur S, Muller C, Pereira de Vasconcelos A, Ballard T, Lopez J, Galani R, Certa U, Cassel JC. 2009. Hippocampal-dependent spatial memory functions might be lateralized in rats: An approach combining gene expression profiling and reversible inactivation. Hippocampus 19:800-816.
30. Kohl MM, Shipton OA, Deacon RM, Rawlins JN, Deisseroth K, Paulsen O. 2011. Hemisphere-specific optogenetic stimulation reveals left-right asymmetry of hippocampal plasticity. Nat Neurosci 14:1413-1415.
31. Levy J, Trevarthen C. 1976. Metacontrol of hemispheric function in human split-brain patients. J Exp Psychol Hum Percept Perform 2:299-312.
32. Liedvogel M, Feenders G, Wada K, Troje NF, Jarvis ED, Mouritsen H. 2007. Lateralized activation of cluster N in the brains of migratory songbirds. Eur J Neurosci 25:1166-1173.
33. Maguire EA, Frackowiak RS, Frith CD. 1997. Recalling routes around london: Activation of the right hippocampus in taxi drivers. J Neurosci 17:7103-7110.
34. Marinkovic K, Dhond RP, Dale AM, Glessner M, Carr V, Halgren E. 2003. Spatiotemporal dynamics of modality-specific and supramodal word processing. Neuron 38:487-497.
35. Marinkovic K, Baldwin S, Courtney MG, Witzel T, Dale AM, Halgren E. 2011. Right hemisphere has the last laugh: Neural dynamics of joke appreciation. Cogn Affect Behav Neurosci 11:113-130.
36. Mehlhorn J, Haastert B, Rehkamper G. 2010. Asymmetry of different brain structures in homing pigeons with and without navigational experience. J Exp Biol 213:2219-2224.
37. Mesulam MM. 1999. Spatial attention and neglect: Parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc Lond B Biol Sci 354:1325-1346.
38. Nardi D, Bingman VP. 2007. Asymmetrical participation of the left and right hippocampus for representing environmental geometry in homing pigeons. Behav Brain Res 178:160-171.
39. Neufang S, Specht K, Hausmann M, Gunturkun O, Herpertz-Dahlmann B, Fink GR, Konrad K. 2009. Sex differences and the impact of steroid hormones on the developing human brain. Cereb Cortex 19:464-473.
40. Ocklenburg S, Gunturkun O. 2012. Hemispheric asymmetries: The comparative view. Front Psychol 3:5-
41. Ocklenburg S, Strockens F, Gunturkun O. 2013. Lateralisation of conspecific vocalisation in non-human vertebrates. Laterality 18:1-31.
42. Pedraza O, Bowers D, Gilmore R. 2004. Asymmetry of the hippocampus and amygdala in MRI volumetric measurements of normal adults. J Int Neuropsychol Soc 10:664-678.
43. Prior H, Gunturkun O. 2001. Parallel working memory for spatial location and food-related object cues in foraging pigeons: Binocular and lateralized monocular performance. Learn Mem 8:44-51.
44. Prior H, Lingenauber F, Nitschke J, Gunturkun O. 2002. Orientation and lateralized cue use in pigeons navigating a large indoor environment. J Exp Biol 205:1795-1805.
45. Pulvermuller F. 2013. Semantic embodiment, disembodiment or misembodiment? In search of meaning in modules and neuron circuits. Brain Lang 127:86-103.
46. Regolin L, Garzotto B, Rugani R, Pagni P, Vallortigara G. 2005. Working memory in the chick: Parallel and lateralized mechanisms for encoding of object- and position-specific information. Behav Brain Res 157:1-9.
47. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Gunturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED, Avian Brain Nomenclature F. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
48. Shanahan M, Bingman VP, Shimizu T, Wild M, Gunturkun O. 2013. Large-scale network organization in the avian forebrain: A connectivity matrix and theoretical analysis. Front Comput Neurosci 7:89.
49. Shinohara Y, Hirase H, Watanabe M, Itakura M, Takahashi M, Shigemoto R. 2008. Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc Natl Acad Sci U S A 105:19498-19503.
50. Shinohara Y, Hosoya A, Yamasaki N, Ahmed H, Hattori S, Eguchi M, Yamaguchi S, Miyakawa T, Hirase H, Shigemoto R. 2012. Right-hemispheric dominance of spatial memory in split-brain mice. Hippocampus 22:117-121.
51. Shipton OA, El-Gaby M, Apergis-Schoute J, Deisseroth K, Bannerman DM, Paulsen O, Kohl MM. 2014. Left-right dissociation of hippocampal memory processes in mice. Proc Natl Acad Sci U S A 111:15238-15243.
52. 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 16:125-140.
53. Siegel M, Donner TH, Engel AK. 2012. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121-134.
54. Specht K. 2014. Neuronal basis of speech comprehension. Hear Res 307:121-135.
55. Strockens F, Gunturkun O, Ocklenburg S. 2013. Limb preferences in non-human vertebrates. Laterality 18:536-575.
56. Thompson DK, Wood SJ, Doyle LW, Warfield SK, Egan GF, Inder TE. 2009. MR-determined hippocampal asymmetry in full-term and preterm neonates. Hippocampus 19:118-123.
57. Tommasi L, Vallortigara G. 2001. Encoding of geometric and landmark information in the left and right hemispheres of the avian brain. Behav Neurosci 115:602-613.
58. Tommasi L, Gagliardo A, Andrew RJ, Vallortigara G. 2003. Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus. Eur J Neurosci 17:1695-1702.
59. Ulrich C, Prior H, Duka T, Leshchins'ka I, Valenti P, Gunturkun O, Lipp HP. 1999. Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav Brain Res 104:169-178.
60. Unver E, Gunturkun O. 2014. Evidence for interhemispheric conflict during meta-control in pigeons. Behav Brain Res 270:146-150.
61. Urgesi C, Bricolo E, Aglioti SM. 2005. Hemispheric metacontrol and cerebral dominance in healthy individuals investigated by means of chimeric faces. Brain Res Cogn Brain Res 24:513-525.
62. Valencia-Alfonso CE, Verhaal J, Gunturkun O. 2009. Ascending and descending mechanisms of visual lateralization in pigeons. Philos Trans R Soc Lond B Biol Sci 364:955-963.
63. Vallesi A, Crescentini C. 2011. Right fronto-parietal involvement in monitoring spatial trajectories. Neuroimage 57:558-564.
64. Vallortigara G, Feruglio M, Sovrano VA. 2005. Reorientation by geometric and landmark information in environments of different size. Dev Sci 8:393-401.
65. Verhaal J, Kirsch JA, Vlachos I, Manns M, Gunturkun O. 2012. Lateralized reward-related visual discrimination in the avian entopallium. Eur J Neurosci 35:1337-1343.
66. Wang D, Buckner RL, Liu H. 2014. Functional specialization in the human brain estimated by intrinsic hemispheric interaction. J Neurosci 34:12341-12352.
67. Wiltschko W, Traudt J, Gunturkun O, Prior H, Wiltschko R. 2002. Lateralization of magnetic compass orientation in a migratory bird. Nature 419:467-470.
68. Woolard AA, Heckers S. 2012. Anatomical and functional correlates of human hippocampal volume asymmetry. Psychiatry Res 201:48-53.