An attempt to develop an operant conditioning paradigm to test for magnetic discrimination behavior in a migratory songbird

Abstract

Birds are thought to possess two magnetosensory systems: (1) a chemical sensor in the bird’s eye, and (2) a magnetoreceptor innervated by the ophthalmic branch of the trigeminal nerve (V1) and presumably located in the upper beak. It has been recently demonstrated that the visually mediated magnetosensory system is crucial to the magnetic compass of the European Robin (Erithacus rubecula). In contrast, the trigeminal nerve system, despite neuronal responses to magnetic stimuli, is neither necessary nor sufficient for magnetic compass orientation in this species. Unfortunately, the potential role of the trigeminal organ is unlikely to be elucidated by the classical behavioral paradigm of the orientation cage, because it tests only for spontaneous compass responses. An operant conditioning study by Mora et al. (Nature 432:508–511, 2004) demonstrated that Homing Pigeons can be conditioned to discriminate the presence and absence of a strong gradient magnetic field stimulus. This discrimination depended on intact ophthalmic branches of the trigeminal nerves. Here, we report detailed attempts aimed at adapting the behavioral paradigm used by the above study for a model migratory bird, the European Robin. We tested three variants of a conditioning procedure very similar to that of Mora et al. (Nature 432:508–511, 2004). Despite extensive training, we were not able to demonstrate that our experimental birds were able to discriminate the magnetic stimuli presented to them. This was, however, not due to a general unsuitability of the conditioning setup for this species, because the robins were able to successfully discriminate the presence and absence of an auditory stimulus in the same setup.

Zusammenfassung

Ansätze zur Entwicklung eines operanten Konditionierungsparadigmas zur Untersuchung der Magnetperzeption eines ziehenden Singvogels

Nach derzeitigem Forschungsstand verfügen Vögel vermutlich über zwei magnetosensorische Systeme: einen quantenphysikalisch begreiflichen Mechanismus im Vogelauge, und einen mit dem Trigiminalnerv assoziierten Sensor im Oberschnabel. Aktuelle Studien konnten zeigen, dass der magnetischen Kompass von Rotkehlchen (Erithacus rubecula) auf dem visuellen System basiert, und bestärken somit den erstgenannten Mechanismus. Im Gegensatz dazu scheint das mit dem Trigeminalnerv assoziierte System dieser Art weder notwendig noch ausreichend zur Detektion der Kompassrichtung zu sein. Indes bestehen Hinweise, dass über diesen Nerv Magnetfeldinformationen vermittelt werden. Welche Rolle das trigeminale System für die Orientierung der Vögel spielt wird mit den klassischen Trichterexperimenten kaum zu beantworten sein, da dieses Paradigma allein auf spontaner gerichteter lokomotorischer Aktivität der Vögel während der Zugzeit basiert. Eine operante Konditionierungsstudie von Mora et al. (Nature 432:508–511, 2004) zeigte, dass Brieftauben auf die Unterscheidung zwischen der An- und Abwesenheit eines starken Magnetstimulus konditioniert werden konnten. Diese Unterscheidung war abhängig von einem intakten ophthalmischen Ast des trigeminalen Nervs. In der vorliegenden Studie beschreiben wir detaillierte Versuche, das von Mora et al. (Nature 432:508–511, 2004) beschriebenen Paradigma auf eine Zugvogelart (Rotkehlchen) zu übertragen. Dafür haben wir drei verschiedene Konditionierungsvarianten durchgeführt. Trotz langer Trainingsperioden waren wir nicht in der Lage die Tiere auf unterschiedliche Magnetstimuli zu konditionieren. Offenkundig lag dies jedoch nicht an dem Paradigma selbst, da die Konditionierung auf auditorische Stimuli mit dem gleichen Versuchsaufbau erfolgreich verlief.

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Acknowledgments

We are most grateful to the following people for helping us in this study: the staff at the University of Oldenburg workshop, who built and maintained our experimental equipment; Dr. Russell Mora, who designed, custom-wrote, and supported the software used to automate our conditioning procedures; various members of the Animal Physiology and Behaviour Laboratory (AG Zoophysiologie und Verhalten), especially Prof. Dr. G. Klump, Dr. Ulrike Langemann and Nina Pohl, who generously let us perform some of the experiments in their laboratory, supplied us with equipment to produce and measure the auditory stimuli used in experiment III, and gave practical advice; all members of the Animal Navigation Laboratory (AG Neurosensorik) for their assistance with this study. This work has been supported by funds from the German Academic Exchange Service (DAAD: a 10-month scientific visit fellowship to D. K.), International Graduate School for Neurosensory Science and Systems (a Ph.D. fellowship to D. K.), Alexander von Humboldt Stiftung (GAFOS-Connect Scholarship to C. V. M.), and a Lichtenberg Grant from Volkswagen-Stiftung (to H. M.). All the experiments comply with the current laws of Germany, where they all were performed. The authors declare that they have no conflict of interest.

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Correspondence to D. Kishkinev.

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Communicated by F. Bairlein.

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Kishkinev, D., Mouritsen, H. & Mora, C.V. An attempt to develop an operant conditioning paradigm to test for magnetic discrimination behavior in a migratory songbird. J Ornithol 153, 1165–1177 (2012). https://doi.org/10.1007/s10336-012-0847-x

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Keywords

  • European Robin
  • Magnetoreception
  • Operant conditioning
  • Magnetic stimulus
  • Navigation