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Dendritic Integration in Olfactory Bulb Granule Cells Dendritic integration in olfactory bulb granule cells: Thresholds for lateral inhibition and role of active conductances upon 3D multi-site photostimulation of spines using a holographic projector module Dissertation Zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) der Fakultät für Biologie und Vorklinische Medizin der Universität Regensburg Vorgelegt von Max Müller aus Nördlingen Januar 2020 - II - Das Promotionsgesuch wurde eingereicht am Die Arbeit wurde angeleitet von Prof. Dr. Veronica Egger. Unterschrift: • III - - IV - Kurzfassung der Arbeit Die GABAergen inhibitorischen axonlosen Körnerzellen (GCs) bilden über lange Dornfortsätze (Spines) reziproke dendrodendritische Synapsen mit Mitral- und Büschelzellen (MC/TCs), den wichtigsten Projektionsneuronen des Riechkolbens von Säugern (Bulbus Olfactorius, OB), aus. Diese Synapsen vermitteln die Selbstinhibition von und laterale Inhibition zwischen MC/TCs. Diese dient der Kontrastverstärkung zwischen ähnlichen Geruchssignalen und der Synchronisation oszillatorischer Aktivität. GCs sind also wesentlich an der Geruchssignalverarbeitung beteiligt. GC-Dendriten sind auf vielfältige Weise hoch erregbar: Synaptische Inputs an einzelnen Spines können Natrium (Na+)-vermittelte Zacken im Membranpotential (Spikes) erzeugen, die auf den Kopf des Spines begrenzt sind und zur reziproken Ausschüttung des Neurotransmitters GABA führen. Eine stärkere Aktivierung führt zu einer globalen Ausbreitung dendritischer Signale, die sowohl niederschwellige Kalzium (Ca2+)- Spikes als auch Na+-Spikes umfassen. Da das Erreichen der globalen Schwellenpotentiale gleichzeitig das Erreichen der Schwelle zu lateraler Inhibition bedeutet, war das Ziel meiner Arbeit, den genauen Übergang von der lokalen zur globalen Signalgebung zu untersuchen: Wie viele Spines, in welcher Position und Verteilung auf dem dendritischen Baum, müssen aktiviert werden, um globale Spikes auszulösen und was sind die molekularen Hauptakteure, sprich welche Ionenkanäle sind beteiligt. Um dies optimal zu untersuchen, haben wir im ersten Teil meiner Arbeit einen holographischen Projektor in das bestehende kommerzielle zwei-Photonen (2P) Galvanometer-basierte 2D-Laser- Scanning-Mikroskop mit einer Uncaging-Einheit (Uncaging: Aktivierung photolabiler biologisch inaktiver Derivate von Neurotransmittern mittels Photolyse) implementiert, der die gleichzeitige Photostimulation mehrerer Spines in drei Dimensionen (3D) in akuten Hirnschnitten ermöglicht. 2P-Uncaging in definierten Mustern mittels holographischer Illumination ist eine leistungsfähige Methode zur Untersuchung neuronaler Funktion, da sie in der Lage ist, mehrere synaptische Inputs in verschiedenen Brennebenen gleichzeitig zu emulieren. Wie bei jedem optischen System haben jedoch auch holographische Projektoren ein begrenztes Produkt aus Raum und Bandbreite, was den räumlichen Bereich – oder das Sichtfeld (FOV) – definierter Illumination für eine gewünschte Auflösung einschränkt. Dieser Kompromiss zwischen holographischem FOV und • V - Auflösung schränkt die Reichweite hochauflösender 2P-Uncaging an Spines auf einzelne Teile des dendritischen Baums ein. Wir erweitern das zugängliche FOV, indem wir mit Hilfe der Galvanometer-Scannerspiegel das holographische FOV beliebig über das abbildende FOV positionieren. Das Projektor-System nutzt die im Mikroskop integrierten Bildfunktionen. Die genauen Positionen der Stimulationspunkte können innerhalb eines erfassten 3D-Bildstapels ausgewählt werden (das Volumen von Interesse, VOI). Der holographische Projektor erzeugt dann 3D-Illuminationsmuster mit Hilfe von mehreren Uncaging Fokussen. Das bildgebende FOV unseres Systems ist 800×800 μm2, innerhalb dessen ein holographisches VOI von 70×70×70 μm3 an beliebigen Positionen ausgewählt und auch während des Experiments bewegt werden kann, ohne die Probe selbst zu bewegen. Wir beschreiben detailliert das Design und das Laserausrichtungsprotokoll sowie das individuell angepasste Software-Plugin, das die 3D- Positionierung von Stimulationspunkten steuert. Um die neurobiologische Anwendung grundsätzlich zu demonstrieren, habe ich die Funktion des holographischen Systems zuerst durch Photolyse von „caged“ Glutamat an den Spines entlang der basalen Dendriten kortikaler Pyramidenzellen (PC) in Hirnschnitten junger Ratten getestet. Über Patchpipetten am Zellkörper (Soma) wurden die Zellen mit kalziumempfindlichem Fluoreszenzfarbstoff (OGB-1) gefüllt und elektrische Potentiale aufgezeichnet. Simultanes Uncaging von Glutamat an mehreren Spines führte zur supralinearen Summation postsynaptischer Potentiale am Soma und schließlich zu Aktionspotentialen. Gleichzeitig zeigte ich die Möglichkeit einer 2P-Ca2+-Bildgebung in 2D im Dendriten und ausgewählten Spines, um damit synaptischen Ca2+ Einfluss, sowie lokale regenerative Ereignisse wie lokale dendritische Spikes aufzuzeichnen. Im zweiten Teil meiner Arbeit wendete ich das System zur Untersuchung dendritischer Integration in GCs an. Wir stellten fest, dass weniger als 10 simultan aktivierte dendrodendritische Spines ausreichen, um lokale und globale dendritische Signale zu erzeugen, die auch lokale Ca2+-Spikes und Na+-Spikes (D-spikes) beinhalten. Obwohl das GC-Ruhepotential im Vergleich zu PCs um ca. -10 mV hyperpolarisiert ist, benötigt das Erreichen des AP- Schwellenpotentials eine ähnliche Anzahl von aktivierten Spines (9,0 ± 1,6 in GCs vs 10 ± 1 in PCs), wobei 5,5 ± 2,1 aktivierte Spines bereits ausreichen, um einen lokalen Ca2+-Spike auszulösen. Die dendritische Integration unterhalb der AP-Schwelle ist meist linear. Bei der Stimulation von 6,5 ± - VI - 2,7 Spines zeigten jedoch ∼ 65 % der GCs supralineare Integration, wobei häufig D-spikes auftraten. Einzelne Spines können die Übergänge zwischen den drei Spikes durch schrittweise erhöhten Ca2+-Einfluss erfassen, was vermutlich zur Erhöhung der Freisetzungswahrscheinlichkeit von GABA führt. Außerdem bewirken die einzelnen Spikes eine zunehmend größere Ausbreitung im Dendriten, was zeigt, dass GCs, abhängig vom Input, zu kompartmentalisierter und globaler Signalgebung fähig sind. Durch pharmakologisches Blockieren verschiedener Ionenkanäle zeigten wir, dass NMDA-Rezeptoren stark zur aktiven Integration beitragen. Morphologische Parameter und die Verteilung der aktivierten Spines auf dem Dendriten spielen dagegen kaum eine Rolle. Zusammenfassend ist festzustellen, dass Dendriten von GCs zu komplexen Rechenleistungen fähig und Schwellenwerte für die GC-vermittelte laterale Inhibition niedrig sind. • VII - - VIII - List of Publications This cumulative dissertation is composed of the following published or submitted manuscripts, in which I am either first or shared co-first author: A. Go, M.A., Mueller, M., Castanares, M.L., Egger, V., and Daria, V.R. (2019). A compact holographic projector module for high-resolution 3D multi-site two-photon photostimulation. PLoS One 14, e0210564. B. Mueller, M., Egger, V. (2020). Dendritic integration in olfactory bulb granule cells: Thresholds for lateral inhibition and role of active conductances upon simultaneous activation. In submission for publication, preprint on BioRxiv. In the course of this work, I contributed to a further publication, which is not part of the dissertation: C. Aghvami, S.S., Mueller, M., Araabi, B.N., and Egger, V. (2019). Coincidence Detection within the Excitable Rat Olfactory Bulb Granule Cell Spines. J Neurosci 39, 584-595. • IX - - X - Personal Contributions Publication A The research was designed by myself, Mary Ann Go, Veronica Egger and Vincent R. Daria. Incorporation of the holographic projector module was done by myself, Mary Ann Go and Michael L. Castañares. Development of the custom software was done by Mary Ann Go. Experimental work was done by myself. The work was supervised by Veronica Egger and Vincent R. Daria, and the publication was written by myself, Mary Ann Go, Michael L. Castañares, Veronica Egger and Vincent R. Daria. Publication B The research was designed and the experimental work was performed by myself. The work was supervised by Veronica Egger. The publication was written by myself and Veronica Egger. Publication C The research was designed by Veronica Egger and Sara S. Aghvami. The experimental work was designed and performed by myself. Simulations were done by Sara S. Aghvami. The work was supervised by Veronica Egger. The publication was written by Sara S. Aghvami and Veronica Egger. • XI - - XII - Table of Contents KURZFASSUNG DER ARBEIT .............................................................................................................. V LIST OF PUBLICATIONS .................................................................................................................... IX PERSONAL CONTRIBUTIONS ........................................................................................................... XI TABLE OF CONTENTS .....................................................................................................................XIII 1 GENERAL INTRODUCTION ........................................................................................................ 1 1.1 Olfaction ....................................................................................................................................................... 1 1.1.1 From the nasal cavity to the cortex: an overview ...................................................................................... 2 1.1.2 The main olfactory bulb .............................................................................................................................
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