Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Original Paper

Functional Connectivity Pattern of the Internal Hippocampal Network in Awake Pigeons: A Resting-State fMRI Study

Behroozi M.a · Ströckens F.a · Stacho M.a · Güntürkün O.a, b

Author affiliations

aDepartment of Biopsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Bochum, Germany; bStellenbosch Institute for Advanced Study (STIAS)/Wallenberg Research Centre at Stellenbosch University, Stellenbosch, South Africa

Related Articles for ""

Brain Behav Evol 2017;90:62-72

Do you have an account?

Login Information





Contact Information












By signing up for MyKarger you will automatically participate in our year-End raffle.
If you Then Do Not wish To participate, please uncheck the following box.

Yes, I wish To participate In the year-End raffle And Get the chance To win some Of our most interesting books, And other attractive prizes.


I have read the Karger Terms and Conditions and agree.



Login Information





Contact Information












By signing up for MyKarger you will automatically participate in our year-End raffle.
If you Then Do Not wish To participate, please uncheck the following box.

Yes, I wish To participate In the year-End raffle And Get the chance To win some Of our most interesting books, And other attractive prizes.


I have read the Karger Terms and Conditions and agree.



To view the fulltext, please log in

To view the pdf, please log in

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

CHF 38.00 *
EUR 35.00 *
USD 39.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.


Save over 20% compared to the individual article price.
Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply

Rental: USD 8.50
Cloud: USD 20.00


Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Published online: September 04, 2017
Issue release date: September 2017

Number of Print Pages: 11
Number of Figures: 3
Number of Tables: 0

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

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

Abstract

In the last two decades, the avian hippocampus has been repeatedly studied with respect to its architecture, neurochemistry, and connectivity pattern. We review these insights and conclude that we unfortunately still lack proper knowledge on the interaction between the different hippocampal subregions. To fill this gap, we need information on the functional connectivity pattern of the hippocampal network. These data could complement our structural connectivity knowledge. To this end, we conducted a resting-state fMRI experiment in awake pigeons in a 7-T MR scanner. A voxel-wise regression analysis of blood oxygenation level-dependent (BOLD) fluctuations was performed in 6 distinct areas, dorsomedial (DM), dorsolateral (DL), triangular shaped (Tr), dorsolateral corticoid (CDL), temporo-parieto-occipital (TPO), and lateral septum regions (SL), to establish a functional connectivity map of the avian hippocampal network. Our study reveals that the system of connectivities between CDL, DL, DM, and Tr is the functional backbone of the pigeon hippocampal system. Within this network, DM is the central hub and is strongly associated with DL and CDL BOLD signal fluctuations. DM is also the only hippocampal region to which large Tr areas are functionally connected. In contrast to published tracing data, TPO and SL are only weakly integrated in this network. In summary, our findings uncovered a structurally otherwise invisible architecture of the avian hippocampal formation by revealing the dynamic blueprints of this network.

© 2017 S. Karger AG, Basel


References

  1. Atoji Y, Sarkar S, Wild JM (2016): Proposed homology of the dorsomedial subdivision and V-shaped layer of the avian hippocampus to Ammon's horn and dentate gyrus, respectively. Hippocampus 26:1608-1617.
  2. Atoji Y, Wild JM (2004): Fiber connections of the hippocampal formation and septum and subdivisions of the hippocampal formation in the pigeon as revealed by tract tracing and kainic acid lesions. J Comp Neurol 475:426-461.
  3. Atoji Y, Wild JM (2005): Afferent and efferent connections of the dorsolateral corticoid area and a comparison with connections of the temporo-parieto-occipital area in the pigeon (Columba livia). J Comp Neurol 485:165-182.
  4. Atoji Y, Wild JM (2014): Efferent and afferent connections of the olfactory bulb and prepiriform cortex in the pigeon (Columba livia). J Comp Neurol 522:1728-1752.
  5. Atoji Y, Wild JM, Yamamoto Y, Suzuki Y (2002): Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J Comp Neurol 447:177-199.
  6. Bingman VP, Casini G, Nocjar C, Jones TJ (1994): Connections of the piriform cortex in homing pigeons (Columba livia) studied with fast blue and WGA-HRP. Brain Behav Evol 43:206-218.
  7. Bingman VP, Gagliardo A, Hough GE, Ioalé 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.
  8. Bingman VP, Salas C, Rodriguez F: Evolution of the hippocampus (2009): in Binder MD, Hirokawa N, Windhorst U (eds): Encyclopedia of Neuroscience. Berlin, Springer, pp 1356-1360.
  9. Casini G, Bingman VP, Bagnoli P (1986): Connections of the pigeon dorsomedial forebrain studied with WGA-HRP and 3H-proline. J Comp Neurol 245:454-470.
  10. Cheng M, Chaiken M, Zuo M, Miller H (1999): Nucleus taenia of the amygdala of birds: anatomical and functional studies in ring doves (Streptopelia risoria) and European starlings (Sturnus vulgaris). Brain Behav Evol 53:243-270.
  11. Daliri MR, Behroozi M (2014): Advantages and disadvantages of resting state functional connectivity magnetic resonance imaging for clinical applications. OMICS J Radiology 3:e123.
  12. De Groof G, Jonckers E, Güntürkün O, Denolf P, Van Auderkerke J, Van der Linden A (2013): Functional MRI and functional connectivity of the visual system of awake pigeons. Behav Brain Res 239:43-50.
  13. Di Martino A, Scheres A, Margulies DS, Kelly AMC, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008): Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18:2735-2747.
  14. Eklund A, Nichols TE, Knutsson H (2016): Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci USA 113:7900-7905.
  15. Erichsen JT, Bingman VP, Krebs JR (1991): The distribution of neuropeptides in the dorsomedial telencephalon of the pigeon (Columba livia): a basis for regional subdivisions. J Comp Neurol 314:478-492.
  16. Fox MD, Raichle ME (2007): Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700-711.
  17. Gagliardo A, Ioalè 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.
  18. 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.
  19. Güntürkün O, Verhoye M, De Groof G, 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.
  20. Herold C, Bingman VP, Ströckens F, Letzner S, Sauvage M, Palomero-Gallagher N, Zilles K, Güntürkün 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.
  21. Herold C, Coppola VJ, Bingman VP (2015): The maturation of research into the avian hippocampal formation: recent discoveries from one of the nature's foremost navigators. Hippocampus 25:1193-1211.
  22. Hough GE, Pang KCH, Bingman VP (2002): Intrahippocampal connections in the pigeon (Columba livia) as revealed by stimulation evoked field potentials. J Comp Neurol 452:297-309.
  23. Hurwitz R, Lane SR, Bell RA, Brant-Zawadzki MN (1989): Acoustic analysis of gradient-coil noise in MR imaging. Radiology 173:545-548.
  24. Husband SA, Shimizu T (1999): Efferent projections of the ectostriatum in the pigeon (Columba livia). J Comp Neurol 406:329-345.
  25. Jenkinson M, Bannister P, Brady M, Smith S (2002): Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17:825-841.
  26. Jonckers E, Güntürkün O, De Groof G, Van der Linden A, Bingman VP (2015): Network structure of functional hippocampal lateralization in birds. Hippocampus 25:1418-1428.
  27. Kahn MC, Hough GE, Ten Eyck GR, Bingman VP (2003): Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: an anterograde and retrograde tracer study. J Comp Neurol 459:127-141.
  28. Kaplan R, Adhikari MH, Hindriks R, Mantini D, Murayama Y, Logothetis NK, Deco G (2016): Hippocampal sharp-wave ripples influence selective activation of the default mode network. Curr Biol 26:686-691.
  29. Karten HJ, Hodos W (1967): Stereotaxic atlas of the brain of the pigeon (Columba livia). Baltimore, Johns Hopkins University Press.
  30. Kröner S, Güntürkün O (1999): Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): a retro- and anterograde pathway tracing study. J Comp Neurol 407:228-260.
  31. Leutgeb S, Mizumori SJ (1999): Excitotoxic septal lesions result in spatial memory deficits and altered flexibility of hippocampal single-unit representations. J Neurosci 19:6661-6672.
  32. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001): Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
  33. Manns M, Freund N, Patzke N, Güntürkün O (2007): Organization of telencephalotectal projections in pigeons: impact for lateralized top-down control. Neuroscience 144:645-653.
  34. Mouritsen H, Heyers D, Güntürkün O (2016): The neural basis of long-distance navigation in birds. Annu Rev Physiol 78:133-154.
  35. 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.
  36. Nasrallah FA, To XV, Chen D-Y, Routtenberg A, Chuang K-H (2016): Functional connectivity MRI tracks memory networks after maze learning in rodents. NeuroImage 127:196-202.
  37. Patzke N, Manns M, Güntürkün O (2011): Telencephalic organization of the olfactory system in homing pigeons (Columba livia). Neuroscience 194:53-61.
  38. Prior H, Wiltschko R, Stapput K, Güntürkün O, Wiltschko W (2004): Visual lateralization and homing in pigeons. Behav Brain Res 154:301-310.
  39. Rattenborg NC, Martinez-Gonzalez D (2011): A bird-brain view of episodic memory. Behav Brain Res 222:236-245.
  40. Robinson J, Manseau F, Ducharme G, Amilhon B, Vigneault E, Mestikawy SE, Williams S (2016): Optogenetic activation of septal glutamatergic neurons drive hippocampal theta rhythms. J Neurosci 36:3016-3023.
  41. Shanahan M, Bingman VP, Shimizu T, Wild M, Güntürkün O (2013): Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis. Front Comput Neurosci 7:89.
  42. Shimizu T, Cox K, Karten HJ (1995): Intratelencephalic projections of the visual wulst in pigeons (Columba livia). J Comp Neurol 359:551-572.
  43. Siegel JJ, Nitz D, Bingman VP (2002): Electrophysiological profile of avian hippocampal unit activity: a basis for regional subdivisions. J Comp Neurol 445:256-268.
  44. Siegel JJ, Nitz D, Bingman VP (2005): Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons. Hippocampus 15:26-40.
  45. Smith SM, Nichols TE (2009): Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44:83-98.
  46. Smulders TV (2017) The avian hippocampal formation and the stress response. Brain Behav Evol 90:81-91.
  47. Song X-W, Dong Z-Y, Long X-Y, Li S-F, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011): REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031.
  48. Stacho M, Letzner S, Theiss C, Manns M, Güntürkün O (2016): A GABAergic tecto-tegmento-tectal pathway in pigeons. J Comp Neurol 524:2886-2913.
  49. Strange BA, Witter MP, Lein ES, Moser EI (2014): Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655-669.
  50. Striedter GF (2016): Evolution of the hippocampus in reptiles and birds. J Comp Neurol 524:496-517.
  51. Tömböl T, Davies DC, Németh A, Sebestény T, Alpár A (2000a): A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat Embryol (Berl) 201:85-101.
  52. Tömböl T, Davies DC, Németh A, Alpár A, Sebestény T (2000b): A Golgi and a combined Golgi/GABA immunogold study of local circuit neurons in the homing pigeon hippocampus. Anat Embryol (Berl) 201:181-196.
  53. Treves A, Tashiro A, Witter MP, Moser EI (2008): What is the mammalian dentate gyrus good for? Neuroscience 154:1155-1172.
  54. Ulrich C, Prior H, Duka T, Leshchins'ka I, Valenti P, Güntürkün O, Lipp HP (1999): Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav Brain Res 104:169-178.
  55. Vandecasteele M, Varga V, Berényi A, Papp E, Barthó P, Venance L, Freund TF, Buzsáki G (2014): Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc Natl Acad Sci USA 111:13535-13540.
  56. van den Heuvel MP, Hulshoff Pol HE (2010): Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519-534.
  57. Winson J (1978): Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160-163.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Published online: September 04, 2017
Issue release date: September 2017

Number of Print Pages: 11
Number of Figures: 3
Number of Tables: 0

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

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


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.