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Synchronization by Distal Dendrite-Targeting Interneurons

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Synchronization by Distal Dendrite-Targeting Interneurons BRAIN INSTITUTE Federal University of Rio Grande do Norte Synchronization by Distal Dendrite-targeting Interneurons - phenomenon, concept and reality - THESIS for the degree of Doctor of Philosophy in Neuroscience submitted by Markus Michael Hilscher Matriculation: 2013116277 at the Brain Institute of the Federal University of Rio Grande do Norte Advisor: Dr. Emelie Katarina Svahn Leão Brain Institute, Federal University of Rio Grande do Norte, Brazil Co-Advisor: Dr. Richardson Naves Leão Brain Institute, Federal University of Rio Grande do Norte, Brazil Co-Advisor: Dr. Klas Kullander Department of Neuroscience, Uppsala University, Sweden Opponent: Dr. Christopher Kushmerick Institute of Biological Sciences, Federal University of Minas Gerais, Brazil Opponent: Dr. Gilad Silberberg Department of Neuroscience, Karolinska Institute, Sweden Natal, 01.04.2017 Federal University of Rio Grande do Norte 59056-450 Natal Av. Nascimento de Castro, 2155 www.neuro.ufrn.br BRAIN INSTITUTE Federal University of Rio Grande do Norte Sincronização através de interneurônios que inervam dendritos distais - fenômeno, conceito e realidade - TESE para a obtenção do título de Doutor em Neurociências apresentada por Markus Michael Hilscher Matrícula 2013116277 no Instituto do Cérebro da Universidade Federal do Rio Grande do Norte Orientadora: Dra. Emelie Katarina Svahn Leão Instituto do Cérebro, Universidade Federal do Rio Grande do Norte, Brasil Co-Orientador: Dr. Richardson Naves Leão Instituto do Cérebro, Universidade Federal do Rio Grande do Norte, Brasil Co-Orientador: Dr. Klas Kullander Departamento de Neurociências, Universidade de Uppsala, Suécia Avaliador: Dr. Christopher Kushmerick Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brasil Avaliador: Dr. Gilad Silberberg Departamento de Neurociências, Instituto Karolinska, Suécia Natal, 01.04.2017 Federal University of Rio Grande do Norte 59056-450 Natal Av. Nascimento de Castro, 2155 www.neuro.ufrn.br Universidade Federal do Rio Grande do Norte - UFRN Sistema de Bibliotecas - SISBI Catalogação de Publicação na Fonte. UFRN - Biblioteca Setorial Árvore do Conhecimento - Instituto do Cérebro - ICE Hilscher, Markus Michael. Synchronization by Distal Dendrite-targeting Interneurons / Markus Michael Hilscher. - Natal, 2017. 152f.: il. Universidade Federal do Rio Grande do Norte, Instituto do Cérebro, PGNeuro. Orientador: Dr. Emelie Katarina Svahn Leão. Coorientador: Dr. Richardson Naves Leão. 1. Synchronization. 2. Hippocampus. 3. OLM cells. 4. Neocortex. 5. Martinotti cells. I. Leão, Emelie Katarina Svahn. II. Leão, Richardson Naves. III. Título. RN/UF/BSICe CDU 612.8 Abstract Synchronization among neurons arises from the cooperative interaction of various cell types through excitation and inhibition. The mechanisms behind this type of neuronal orchestration are as versatile as almost no other coordination task in the brain, making its comprehension heavily challenging. Among many others, the high number of involved cell types, the diversity of synaptic processes as well as the contribution of a multitude of ion channels and currents span the plurality of neuronal synchronization mechanisms in our brains. Focusing on two brain ar- eas, the hippocampus and the neocortex, this thesis aims to understand the role of distal dendrite- targeting interneurons in shaping pyramidal cell activity and the timing of their action potentials. The distribution of ion channels and synaptic receptors in pyramidal cell dendrites is extremely anisotropic. Thus, interneurons innervating the proximal or distal areas of the dendrites cause different effects in the target cell when activated. For example, the distal portions of the pyrami- dal cell dendrites contain one of the most prominent pacemaker channels: the hyperpolarization- activated cyclic nucleotide-gated channels. These channels produce a cationic depolarizing cur- rent (Ih) and play an essential role in the regulation of neuronal excitability. Using computational modeling, this thesis shows how the amount of Ih in certain cell types determines their spike rate, synchrony as well as power and frequency of ongoing network oscillations. Moreover, since Ih differs between brain regions as well as cell types and location, this thesis electrophysiologically explores how Ih differs along the dorsoventral axis of hippocampus in oriens-lacunosum molec- ulare (OLM) cells, the main distal dendrite-targeting interneurons of that region. Utilizing the main distal dendrite-targeting interneuron of the neocortex, the Martinotti cell, this thesis also shows how a defined population of interneurons can be manipulated in order to con- trol and align pyramidal cell firing. By providing the right amount and frequency of inhibition, Martinotti cells are able to synchronize trains of subtype-specific pyramidal cells. Using opto- genetic approaches to activate/inactivate populations of Martinotti cells, these dendrite-targeting interneurons are shown to trigger rebound action potentials in pyramidal cells when temporally aligned. The rebound action potentials in turn are the result of strong inhibition by Martinotti cells, giving these distal dendrite-targeting interneurons the power to reset pyramidal cell firing. Overall, Martinotti cells and OLM cells show quite striking similarities in morphological, neuro- chemical and electrophysiological properties. Especially, their long axonal projections to upper layers as well as their low-threshold, slow spiking fashion and the accommodating firing make these distal dendrite-targeting interneurons so special for neuronal synchronization. i Resumo A sincronização neuronal surge de uma interação cooperativa de vários tipos celulares através de excitação e inibição. Os mecanismos por trás desse tipo de coordenação neuronal são, prova- velmente, os mais dinâmicos entre as funções cerebrais, dificultando sua compreensão. Entre os fatores que dificultam o estudo da sincronia, pode-se citar: o vasto número de tipos de celulares, a diversidade de processos sinápticos, a contribuição de uma multiplicidade de canais e corren- tes iônicas, entre outros. Essa tese tem como objetivo entender o papel de interneurônios que especificamente inervam o domínio distal dos dendritos de células piramidais do hipocampo e neocórtex, na sincronização de neurônios em suas respectivas redes. A distribuição de canais iônicos e receptors sinápticos em dendritos de células piramidais é ex- tremamente anisotrópica. Assim, interneurônios que inervam domínios proximais e distais dos dendritos causam efeitos distintos na célula alvo quando ativados. Por exemplo, porções dis- tais dos dendritos contém em abundância um dos principais canais marcapassos em neurônios: o canal regulado por nucleotídeo cíclico ativado por hiperpolarização. Esses canais produzem uma corrente catiônica despolarizante (Ih) e tem um papel importante na regulação da excita- bilidade neuronal alterando dramaticamente as propriedades de disparo de neurônios. Usando modelagem computacional, essa tese mostra como a amplitude de Ih em certos tipos celulares muda a taxa de disparo de um neurônio, sua sincronia além da energia espectral e frequência de oscilações. Além disso, como a expressão de Ih difere entre regiões cerebrais, localização e tipos celulares, essa tese, fazendo o uso de patch clamp, explora como Ih difere ao longo do eixo dorsoventral do hipocampo em células oriens-lacunosum moleculare (OLM), que são os principais interneurônios que inervam dendritos distais dessa região. Ademais, estudou-se aqui as células Martinotti, interneurônios que inervam os dendritos dis- tais do neocórtex. Nesse estudo, mostrou-se como uma população definida de interneurônios pode ser manipulada com o objetivo de controlar e coordenar o disparo de células piramidais. Ao fornecer inibição com energia e frequência adequada, as células Martinotti afetam especifica- mente um único tipo de célula piramidal. Usando optogenética para ativar/desativar populações de células Martinotti, é possível gerar potenciais de ação rebote em células piramidais quando alinhadas temporalmente. Os potenciais de ação rebote, por sua vez, são resultado de uma forte inibição produzida pelas células Martinotti, o que faz com que esses esses interneurônios pos- sam resetar o disparo de células piramidais. iii De forma geral, células Martinotti e células OLM mostram similaridades surpreendentes em propriedades morfológicas, neuroquímicas e eletrofisiológicas. Especialmente, suas longas pro- jeções axonais para camadas superiores assim como seus modos de disparo lentos, com baixos limiares e acomodativos tornam esses neurônios singulares em suas capacidades de sincronizar os circuitos nos quais estão inseridos. Kurzfassung Synchronisation zwischen Neuronen entsteht durch das kooperative Zusammenspiel von ver- schiedenen Zelltypen und deren Erregung und Hemmung. Die Mechanismen hinter dieser Art der neuronalen Orchestrierung sind so vielseitig wie kaum ein anderer Koordinierungsprozess im Gehirn. Die große Anzahl an beteiligten Zelltypen, die Vielfalt der synaptischen Prozesse sowie der Beitrag einer Vielzahl von Ionenkanälen und Strömen charakterisieren die neurona- len Synchronisationsmechanismen in unserem Gehirn. Der Schwerpunkt dieser Arbeit liegt auf zwei Bereichen des Gehirns, dem Hippocampus und dem Neocortex, und der Rolle von distalen Dendriten-innervierenden Interneuronen, die Pyramidenzellen steuern und den Zeitpunkt ihrer Aktionspotentiale beeinflussen können. Die Verteilung der Ionenkanäle und synaptischen
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