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Plasticity of the Mauthner-Cell Associated C-Start Circuitry

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Plasticity of the Mauthner-Cell Associated C-Start Circuitry Plasticity of the Mauthner-cell associated C-start circuitry Kumulative Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) der Fakultät für Biologie, Chemie und Geowissenschaften der Universität Bayreuth Vorgelegt von Philipp Krupczynski Bayreuth, im Juni 2014 Die vorliegende Arbeit wurde in der Zeit von Juni 2007 bis Juni 2014 in Bayreuth am Lehrstuhl für Tierphysiologie unter Betreuung von Herrn Prof. Dr. Stefan Schuster angefertigt. Vollständiger Abdruck der von der Fakultät für Biologie, Chemie und Geowissenschaften der Universität Bayreuth genehmigten Dissertation zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.). Dissertation eingereicht am: 24.06.2014 Zulassung durch die Promotionskommission: 02.07.2014 Wissenschaftliches Kolloquium: 05.11.2014 Amtierender Dekan: Prof. Dr. Rhett Kempe Prüfungsausschuss: Prof. Dr. Stefan Schuster (Erstgutachter) Prof. Dr. Gerrit Begemann (Zweitgutachter) Prof. Dr. Christian Laforsch (Vorsitz) Prof. Dr. Benedikt Westermann Für meine Eltern und meine Freundin TABLE OF CONTENTS Zusammenfassung ................................................................................................................. 1! Summary ............................................................................................................................... 3! Introduction ........................................................................................................................... 5! Synopsis .............................................................................................................................. 12! References ........................................................................................................................... 23! Author’s contribution .......................................................................................................... 27! Publications ......................................................................................................................... 29! Precision of archerfish C-starts is fully temperature compensated .............................................. 31! Meta-control ensures accuracy in high-speed decision-making ................................................... 57! Fruit-catching fish tune their fast starts to compensate for drift ................................................... 73! Full adaptive plasticity in a vital circuit of the adult vertebrate brain .......................................... 91! Danksagung ....................................................................................................................... 105! Eidesstattliche Versicherungen und Erklärungen ............................................................. 107! ZUSAMMENFASSUNG ZUSAMMENFASSUNG Das Mauthner (M)-Zellen assoziierte retikulärspinale Netzwerk von Fischen und Kaulquappen erlangte im Wesentlichen aufgrund seiner Zugänglichkeit auf zellulärer Ebene und durch die enorme Größe der zwei M-Zellen Bedeutung in der Neurowissenschaft. Trotz der erstaunlicherweise geringen Größe dieses neuronalen Netzwerks mit nur einigen hundert Zellen und wenigen synaptischen Verbindungen, die von einem Individuum zum nächsten identifiziert werden können, ist es für ein wichtiges Manöver verantwortlich, den Flucht C-start der meisten Knochenfische. Diese Studie trägt wichtige Aspekte zu der Auffassung bei, dass das Flucht-Netzwerk, obwohl klein, hoch anspruchsvolle und plastische C-Start Entscheidungen steuert. In Schützenfischen lenkt es den sogenannten prädiktiven C-Start: Anhand der visuellen Beurteilung der Anfangsbewegung von abgeschossenen, in der Luft frei fallenden Futterobjekten, führen diese Fische einen C-Start aus, der sie perfekt ausgerichtet auf den späteren Auftreffpunkt dreht und sie mit angepasster Geschwindigkeit abstößt, um die Beute zum richtigen Zeitpunkt zu fangen. Die hohe Präzision in Bezug auf den Zielpunkt und die vollständige experimentelle Kontrolle der prädiktiven C-Starts machen diese Entscheidungen zu wertvollen Modellsystemen dafür, wie im Nervensystem Entscheidungen getroffen werden und wie Umwelteinflüsse die zugrundeliegenden Netzwerke beeinflussen. Zusammen mit der Zugänglichkeit der Netzwerke eignen sich diese Starts hervorragend für eine Untersuchung des Ausmaßes der neuronalen Plastizität und der Aufdeckung innewohnender Puffermechanismen für das Erreichen funktioneller Stabilität. Hier lege ich vier zentrale Ergebnisse vor. (1) Funktionale Stabilität. Temperatur beeinflusst die Physiologie poikilothermer Tiere und daher die Eigenschaften ihrer neuronalen Netzwerke, was ihre Leistung beeinträchtigen könnte. Dennoch müssen Schützenfische die richtigen Entscheidungen treffen: die Wahl eines ungeeigneten Drehwinkels oder Startgeschwindigkeit bedeutet den Verlust der Beute an die zahlreichen Konkurrenten. Das Entscheidungs-Netzwerk sollte daher gepuffert werden, so dass die Funktion nicht durch Temperaturveränderungen beeinflusst wird. Tatsächlich konnte ich herausfinden, dass nach einer kurzen Akklimatisierungsphase die Funktion der prädiktiven C-Starts der Schützenfische in einem Temperaturbereich vollständig erhalten blieb. Bei allen Temperaturen wurde die Reaktionsfähigkeit aufrechterhalten, und die Fische wählten genaue Drehungen im gesamten Winkelbereich. Darüber hinaus passten sie mit gleicher Genauigkeit bei allen Temperaturen ihre Startgeschwindigkeit an die verbleibende Distanz zum Auftreffpunkt ihrer Beute und der verbleibenden Zeit bis zum Aufschlag an. Andere Aspekte wie Latenz oder die C-Start Kinematik waren indes nicht oder nur teilweise Temperatur kompensiert. (2) Intrinsische Qualitätssicherung. Verringern der Helligkeit reduziert die Zuverlässig- 1 PLASTICITY OF THE M-CELL CIRCUITRY keit der visuellen Information, auf dessen Grundlage die prädiktiven Starts ausgeführt werden. Basierend auf typischen Befunden vieler Entscheidungen sollte dies zu einem Zerfall der Genauigkeit führen. Jedoch konnte ich herausfinden, dass dies nicht für die Schützenfisch C-Starts zutrifft. Die Schützenfische entschieden sich richtig im gesamten Bereich von Eingangskonstellationen mit konstanter Genauigkeit bis zu einer reduzierten Helligkeit von 5×10–3 cd m–2. Unterhalb dieser Schwelle wurden keine prädiktiven C- Starts ausgelöst, obwohl die Fische bei dieser und weit aus geringeren Lichtverhältnissen nachweislich sehen konnten und präzise auf Beute schossen. Trotz der Verringerung der Auslösewahrscheinlichkeit und gleichzeitigem Anstieg der Latenz (um die Beute- Anfangsbewegung verlängert zu evaluieren), blieben die grundlegenden kinematischen Eigenschaften der C-Starts im Dunklen unverändert. Meine Ergebnisse weisen auf einen Kontrollmechanismus noch unbekannter Natur hin, der sicherstellt, dass C-Starts nur dann ausgelöst werden, wenn sie erwartungsgemäß exakt auf den späteren Auftreffpunkt gerichtet sind. (3) Das Netzwerk wird auch in anderen Arten ähnlich genutzt. Da der Großteil der Knochenfische das M-Zellen assoziierte Netzwerk besitzt, kam die Frage auf, ob andere Arten neben dem Schützenfisch dieses Netzwerk nicht nur für die Flucht, sondern auch für genau abgestimmte Starts in ihrer Ernährungsweise benutzen. Anhand von Feldforschung in Costa Rica stellte ich fest, dass der Früchte fressende, in Flüssen lebende Machaca, Brycon guatemalensis, C-Starts in der Art und Weise wie Schützenfische verwendet. Wartend unterhalb von Bäumen mit reifen Feigen, frontal zur Strömung ausgerichtet, reagieren diese Fische auf die visuelle Information fallender Früchte bevor diese auf die Wasseroberfläche aufschlagen und starten in Richtung des späteren Auftreffpunkts. Der interessante Aspekt dieser Starts ist, dass die Fische (aber nicht ihr Zielobjekt) starker Strömung ausgesetzt sind. Erstaunlicherweise lösten die Fische dieses Problem gleich bei ihrem Start, indem sie sich in eine Richtung drehten, die optimal an die Abdrift auf ihrem Weg zum Ziel angepasst war. (4) Das Netzwerk kann in adulten Zebrafischen neu programmiert werden. Es stellte sich die Frage, ob man noch einen Schritt weiter gehen könnte und das M-Zellen Netzwerk sogar durch zuvor Entscheidungs-irrelevante Information angepasst werden kann. Nachdem adulte Zebrafische ausschließlich einer Umwelt ausgesetzt wurden, in der das gesamte Futter auf ballistischen Flugbahnen aus der Luft fiel, konnten wir zeigen, dass das Netzwerk tatsächlich die Fallgesetze verinnerlicht hatte. Die Zebrafische waren imstande, genau abgestimmte C-Starts für beliebige Flugbahnen auszuwählen, sogar für zuvor völlig unbekannte. Daraus ergibt sich die einmalige Möglichkeit, den Aufbau der Repräsentation eines Physikgesetzes in einem kleinen definierten Netzwerk zu erforschen, und um zu verstehen, wie Gesetze der äußeren Welt in der Sprache der neuronalen Netzwerke dargestellt werden. 2 SUMMARY SUMMARY The Mauthner (M)-cell associated reticulospinal circuitry of fish and tadpoles has been important in neuroscience largely due to its accessibility on a cellular level and due to the enormous size of the two M-cells. Although this neuronal network is surprisingly small with a few hundred defined cells and few synaptic levels that can be identified from one individual to the next, it is responsible for an important manoeuvre, the escape C-start shown by most teleost fish. This study contributes several key issues to argue that the escape circuitry, although small, drives highly sophisticated and plastic C-start decisions. In archerfish it drives their so-called predictive C-start: Based on
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