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UNIVERSIDADE ESTADUAL DE CAMPINAS Instituto De Biologia UNIVERSIDADE ESTADUAL DE CAMPINAS Instituto de Biologia Vinicius Miessler de Andrade Carvalho Description and analysis of olfactory maps in the brain Determinação e análise de mapas olfatórios no cérebro Campinas 2016 VINICIUS MIESSLER DE ANDRADE CARVALHO DESCRIPTION AND ANALYSIS OF OLFACTORY MAPS IN THE BRAIN DETERMINAÇÃO E ANÁLISE DE MAPAS OLFATÓRIOS NO CÉREBRO Thesis presented to the Institute of Biology of the University of Campinas in partial fulfillment of the requirements for the degree of Doctor in Genetics and molecular biology, in the area of Animal genetics and evolution Tese apresentada ao Instituto de Biologia da Universidade Estadual de Campinas como parte dos requisitos exigidos para a obtenção do Título de Doutor em Genética e biologia molecular, na área de Genética animal e evolução. ESTE ARQUIVO DIGITAL CORRESPONDE À VERSÃO FINAL DA TESE DEFENDIDA PELO ALUNO VINICIUS MIESSLER DE ANDRADE CARVALHO E ORIENTADA PELO PROFESSOR DOUTOR FABIO PAPES Orientador: FABIO PAPES CAMPINAS 2016 Agência(s) de fomento e nº(s) de processo(s): FAPESP, 2012/21786-0 Ficha catalográfica Universidade Estadual de Campinas Biblioteca do Instituto de Biologia Mara Janaina de Oliveira - CRB 8/6972 Carvalho, Vinicius Miessler de Andrade, 1989- C253d CarDescription and analysis of olfactory maps in the brain / Vinicius Miessler de Andrade Carvalho. – Campinas, SP : [s.n.], 2016. CarOrientador: Fabio Papes. CarTese (doutorado) – Universidade Estadual de Campinas, Instituto de Biologia. Car1. Órgão vomeronasal. 2. Núcleo hipotalâmico ventromedial. 3. Feromônios. 4. Olfato. 5. Instinto. I. Papes, Fabio,1975-. II. Universidade Estadual de Campinas. Instituto de Biologia. III. Título. Informações para Biblioteca Digital Título em outro idioma: Determinação a análise de mapas olfatórios no cérebro Palavras-chave em inglês: Vomeronasal organ Ventromedial hypothalamic nucleus Pheromones Smell Instinct Área de concentração: Genética Animal e Evolução Titulação: Doutor em Genética e Biologia Molecular Banca examinadora: Fabio Papes [Orientador] Newton Sabino Canteras Lício Augusto Velloso Jörg Kobarg Lisa Stowers Anderson Data de defesa: 31-08-2016 Programa de Pós-Graduação: Genética e Biologia Molecular Powered by TCPDF (www.tcpdf.org) Campinas, 31 de agosto de 2016. COMISSÃO EXAMINADORA Prof. Dr. Fabio Papes Prof.(a). Dr.(a). Lisa Stowers Anderson Prof. Dr. Newton Sabino Canteras Prof. Dr. Lício Augusto Velloso Prof. Dr. Jorg Kobarg Os membros da Comissão Examinadora acima assinaram a Ata de defesa, que se encontra no processo de vida acadêmica do aluno. Aos meus pais Susy e Walter. Acknowledgements To my parents, Susy and Walter, who provided unconditional support for every decision I made and through every step of the way. To my siblings, Priscila, Leonardo, Alexandre and Leticia (who is not actually a sibling, but is like a sister to me) who besides being family, are some of the best friends I could have ever hoped for. To my grandmother, Vovó Telinha, who recently moved in to my house, who is a great partner for card games and who does not hesitate to share her wisdom and experience with me and my siblings. To my companion, Thiara, who was by my side through most of my Ph.D journey, with whom I was able to share the good moments, and who did not leave my side in the bad ones. To my second mother, Eva, for receiving me and supporting me during one of the most important years of my life. To my advisor, Fabio, for believing in me, for teaching me what it means to be a scientist, and for the opportunities provided throughout these four years. To Lisa, who was kind enough to receive me in her lab, for giving me the best possible working conditions for the development of my ideas, and for giving me the opportunity to participate in some of the most rewarding academic experiences I could have ever hoped for, especially the participation in a Janelia Conference. To my first scientific mentor, Joan, for teaching me most of what I know about molecular biology, and for putting me on the right track for a good Ph.D. To all my dear lab partners and friends in Campinas, Thiago, Mateus, Guilherme, Fabio, Felipe, Leonardo C, Antonio, Pedro G, Pedro M, Paulo, Heloísa, for all the talks and discussion about our experiments and experiences, and for all the important afternoon coffee breaks. To the lab technicians, Juliana and Ana Paula, without whom this work would have been nearly impossible to finish. To all my dear lab partners and friends in San Diego, Jason, Han, Sandeepa, Tomo, Eric and Norah, for all the excellent discussions and ideas about science and life in general, that helped me better understand my own project, and for valuing my opinion in their own works. A special thanks to Jason, for the patience to teach me techniques that will be invaluable for my future as a scientist and for receiving me in his house when I needed a place to catch the NBA Finals. To all my wonderful friends, with whom I shared so many good times and memories. Even though time often takes people in different paths that eventually drives them apart, I know I will always remember each of you for the importance you had in my life. I apologize in advance if I forget anyone, but if you know me well enough, you will understand and feel contemplated. Bonis, Bola, Messias, Zeugma, Toba, Saquê, Qualy, Lui, Cuca, Proveta, Maiona, Ema, Pudim, Lux, Gabriel, Suzuki, Taran, Bia, Ace, Guilherme B, Erick, Capela, Rodriguinho, Nick, Dani, Pam, Julio, Bari, Reus, Nikki, A Hong, Mateus, Miki, Gabí, Dudu, Or Pei, Angus Suen, Giano, Mei Mei, Gameboy, Keroro (Fatcheung Lau), Leung Ka Yip, Charmaine, Yannie Ma and Mr. Choi. To my closest friends, Diogo, Bruce, Nove, and Lu. No matter how far life drives us apart, I know I can always count in each one of you. Even at the worst of times, a simple exchange of words with any of you brightened my day. To Professor Gonçalo Pereira and all the LGE team, who welcomed us with open arms into a great work environment. To Professor Newton Canteras and his student Felipe, who welcomed me in their lab, and who helped shed light into my work, when I was unsure of the next step. To Professor Jose Andres Yunes, who shared his resources with our group every time we needed. To the Lactad staff, Felipe and Janine, who were always very helpful and available. To Professor Licio Velloso and his student Roberta, who welcomed me in their lab and helped out when we needed. To Dr. Eliana Ferraz and the Campinas municipal zoo, who were always willing to help, and ensured we had a steady stream of different animal odors. To Getulio, who provided us with all the snake skins we could get our hands on. To FAPESP, who provided financial support that made this work possible. “Curiosity is not a sin… But we should exercise caution with our curiosity… yes, indeed.” Albus Dumbledore in Harry Potter and the Goblet of Fire; J. K. Rowling, 2000 “Nothing in biology makes sense except in the light of evolution” Theodosius Dobzhansky, 1973 Resumo O Sistema nervoso está organizado para detectar, representar e processar a informação sensorial com o intuito de gerar respostas comportamentais e fisiológicas adequadas. Apesar da importância de odores capazes de gerar respostas instintivas, sua representação neural segue pouco caracterizada no cérebro de mamíferos. No presente trabalho analisamos diferentes áreas no cérebro ativadas por uma vasta gama de odores capazes de gerar respostas instintivas (feromônios e cairomônios), e notamos que o cérebro é muito ativado por odores de outras espécies, especialmente predadoras. Quando analisamos o padrão de representação de sinais químicos no núcleo amidalar medial no cérebro, não observamos nenhum tipo de segregação espacial na representação de odores de predadores e conspecíficos, contrariando o atual modelo de organização deste núcleo que implica na existência de dois setores nessa área, relacionadas com comportamentos sociais ou de defesa contra predadores. Surpreendentemente, entretanto, encontramos um mapa organizado da informação olfatória em outro núcleo cerebral, em que diferentes estímulos induzem atividade em neurônios distintos e posicionados de maneira estereotípica no hipotálamo ventromedial. Este padrão de atividade parece não refletir os comportamentos induzidos, e ao invés disso parece representar a identidade dos neurônios ativados no órgão vomeronasal. Estes resultados indicam que padrão de representação de estímulos olfatórios no hipotálamo ventromedial constitui, em contrapartida a um mapa comportamental. O achado surpreendente deste mapa no sistema límbico ajudará a entender como a informação olfatória é processada no cérebro para gerar comportamentos instintivos, em especial, àqueles importantes para a sobrevivência do indivíduo e da espécie. Abstract The nervous system is organized to detect, internally represent and process sensory information to generate appropriate physiological and behavioral responses. Despite the crucial importance of odors that elicit instinctive behaviors, their neural representation remains little characterized in the mammalian brain. In this thesis, we have studied selected brain areas activated by a range of odors capable of eliciting instinctive behaviors (pheromones and kairomones), and found the brain to be exquisitely activated by odors from other species, especially predators. When we analyzed the representation of chemosignals in the medial nucleus of the amygdala in the brain, no spatial segregation in the representation of predator and conspecific odors was observed, contrary to previous models that implicated supposedly distinct sector of this brain area in social and predator defense behaviors. Surprisingly, however, we found a discernibly organized map of olfactory information in another higher brain center, where different stimuli entail activity in distinct and stereotypically positioned groups of neurons in the ventromedial nucleus of the hypothalamus. This activity pattern does not reflect the induced behaviors, as proposed by others, and seems to reflect the molecular receptors involved in the detection of these cues by the vomeronsasal organ.
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