Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus

Detalhes bibliográficos
Autor(a) principal: Luisa Fernanda Ramirez Ochoa
Data de Publicação: 2022
Tipo de documento: Tese
Idioma: eng
Título da fonte: Repositório Institucional da UFMG
Texto Completo: http://hdl.handle.net/1843/57796
https://orcid.org/0000-0002-8052-3260
Resumo: Our success in understanding the retina is partially due to its layered structure, that facilitates the study of circuit motifs and neuronal function. We can understand retinal information processing in three broad stages: I. encoding of light stimuli via electrical signals; II. signal processing by retinal circuits; and III. generation of the retinal code. In this thesis, I focus in the study of the first and third stages from an information-theory perspective. On the first stage, we investigate color coding in zebrafish retinal circuits based on recent experimental findings showing evidence of efficient coding. We propose a theoretical framework to study the encoding performance of different types of outer retinal networks, contrasting the role of excitation and inhibition. More specifically, we use a neuronal population model with chromatic stimulation to study the dynamical properties of such networks. Our findings suggest that inhibition plays a key role in encoding color information reliably, which is not guaranteed in networks with strong excitatory inter-cone couplings. Similarly, we find that networks optimized to encode aquatic spectral information are similar to that observed in zebrafish, providing more general understanding of zebrafish-like retinal circuits of color coding. These results provide quantitative evidence that the zebrafish retina is adapted to efficiently encode information from the environment, enhancing this animal's color vision capabilities. Studies in other species show that animals can adopt different strategies to improve color vision. For instance, in birds and turtles oil droplets serve as a filter to provide a plethora of distinguishable colors. Oil droplets and adapted retinal circuits have been investigated separately. Nevertheless, studies on the combination of both remain unknown. We implement a light transmission model of droplets to investigate the encoding performance of zebrafish-like retinal circuits exhibiting efficient coding. Our findings suggest that introducing droplets in a circuit for chromatic efficient coding creates a trade-off between coding efficiency and color-space gamut. That is, droplets decrease the network encoding performance while increasing the number of distinguishable colors. Regarding the third stage of processing, we focus on the theoretical study of neuronal interactions in the ganglion layer and their compressibility as a path to building simpler models of neuronal activity. Conventional models of neuronal activity introduce assumptions about neural interactions inspired in condensed-matter systems. But these models fail when the number of neurons increases, leading to an exponential explosion in the number of parameters. Here, we implement information theory and renormalization group ideas to explore efficient descriptions of neuronal activity. More specifically, we apply the compression-bottleneck formalism to a population of ganglion cells in the salamander retina. We find that compression leads to a vast simplification in the description of neuronal activity, outperforming conventional pairwise-interaction models. As a generalization, we implement this approach in a population of hippocampus neurons, yielding broadly similar results, suggesting that compressibility is a general feature of spiking neuronal networks.
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spelling Ronald Dickmanhttp://lattes.cnpq.br/0484982277336205William Samuel BialekLucas Lages WardilStephanie Elizabeth PalmerMauro Copelli Lopes da Silvahttp://lattes.cnpq.br/5448393345682958Luisa Fernanda Ramirez Ochoa2023-08-14T15:46:55Z2023-08-14T15:46:55Z2022-12-01http://hdl.handle.net/1843/57796https://orcid.org/0000-0002-8052-3260Our success in understanding the retina is partially due to its layered structure, that facilitates the study of circuit motifs and neuronal function. We can understand retinal information processing in three broad stages: I. encoding of light stimuli via electrical signals; II. signal processing by retinal circuits; and III. generation of the retinal code. In this thesis, I focus in the study of the first and third stages from an information-theory perspective. On the first stage, we investigate color coding in zebrafish retinal circuits based on recent experimental findings showing evidence of efficient coding. We propose a theoretical framework to study the encoding performance of different types of outer retinal networks, contrasting the role of excitation and inhibition. More specifically, we use a neuronal population model with chromatic stimulation to study the dynamical properties of such networks. Our findings suggest that inhibition plays a key role in encoding color information reliably, which is not guaranteed in networks with strong excitatory inter-cone couplings. Similarly, we find that networks optimized to encode aquatic spectral information are similar to that observed in zebrafish, providing more general understanding of zebrafish-like retinal circuits of color coding. These results provide quantitative evidence that the zebrafish retina is adapted to efficiently encode information from the environment, enhancing this animal's color vision capabilities. Studies in other species show that animals can adopt different strategies to improve color vision. For instance, in birds and turtles oil droplets serve as a filter to provide a plethora of distinguishable colors. Oil droplets and adapted retinal circuits have been investigated separately. Nevertheless, studies on the combination of both remain unknown. We implement a light transmission model of droplets to investigate the encoding performance of zebrafish-like retinal circuits exhibiting efficient coding. Our findings suggest that introducing droplets in a circuit for chromatic efficient coding creates a trade-off between coding efficiency and color-space gamut. That is, droplets decrease the network encoding performance while increasing the number of distinguishable colors. Regarding the third stage of processing, we focus on the theoretical study of neuronal interactions in the ganglion layer and their compressibility as a path to building simpler models of neuronal activity. Conventional models of neuronal activity introduce assumptions about neural interactions inspired in condensed-matter systems. But these models fail when the number of neurons increases, leading to an exponential explosion in the number of parameters. Here, we implement information theory and renormalization group ideas to explore efficient descriptions of neuronal activity. More specifically, we apply the compression-bottleneck formalism to a population of ganglion cells in the salamander retina. We find that compression leads to a vast simplification in the description of neuronal activity, outperforming conventional pairwise-interaction models. As a generalization, we implement this approach in a population of hippocampus neurons, yielding broadly similar results, suggesting that compressibility is a general feature of spiking neuronal networks.O nosso sucesso no entendimento da retina se deve em parte à estrutura de camadas que facilita o estudo de diferentes tipos de circuitos e funções neuronais. O processamento de informação na retina pode ser entendido em três etapas: I. Codificação de estímulos visuais em sinais elétricos. II. Processamento desses sinais por circuitos na retina. III. Geração do código retinal. O meu trabalho de tese está focado no estudo da primeira e última etapa desde uma perspectiva da teoria da informação. Na primeira etapa, investigamos a codificação de cor pelos circuitos retinais do zebrafish, baseados em resultados experimentais recentes que mostram evidencia de codificação eficiente. Nós propormos um modelo teórico para estudar codificação em diferentes tipos de redes retinais nas camadas externas, contrastando o papel da excitação e inibição. Os nossos resultados sugerem que a inibição joga um rol importante na codificação reliable de cor, o que não é garantido em redes com fortes interações excitatórias entre cones. De forma similar, os nossos resultados mostram que as redes otimizadas para codificar informação espectral em ambientes aquáticos são similares a aquelas observadas no zebrafish, validando os resultados experimentais e provendo um entendimento mais geral de circuitos retinais para codificação de cor com estruturas similares a aquelas do zebrafish. Estes resultados sugerem que a retina do zebrafish poderia ter se adaptado para fazer uma codificação eficiente da informação do ambiente, melhorando as capacidades de visão colorida. Estudos em outras espécies mostram que os animais podem adoptar diferentes estratégias para melhorar a visão colorida. Por exemplo, em pássaros e tartarugas, a existência de gotas oleosas serve como um filtro para expandir a quantidade de cores distinguíveis. Gotas oleosas e circuitos retinais adaptados tem sido investigados de forma separada. Porém estudos sobre a combinação dos dois continuam desconhecidos. Nós implementamos um modelo de transmissão de luz das gotas para investigar a codificação de circuitos similares a aqueles do zebrafish que mostram uma codificação eficiente. Nossos resultados sugerem que a introdução de gotas oleosas naqueles circuitos gera um trade-off entre codificação eficiente e espaço de cor. Isto é, gotas oleosas diminuem a qualidade de codificação da rede enquanto expandem o numero de cores potencialmente distinguíveis pelo animal. Relacionado à última etapa de processamento retinal, o nosso trabalho se foca no estudo teórico da atividade neuronal na camada ganglionar e a compressibilidade como um caminho para construir modelos simples de atividade neuronal. Modelos convencionais de atividade neuronal fazem suposições sobre interações neuronais inspiradas em sistemas de matéria condensada. Mas, esses modelos falham quando o número de neurônios aumenta, levando a um aumento exponencial no número de parâmetros. Neste trabalho implementamos ideias de teoria de informação de grupo de renormalização para procurar descrições eficientes da atividade neuronal. Mais especificamente, aplicamos o formalismo de compression-bottleneck numa população de células ganglionares na retina da salamandra. Os nossos resultados mostram que a compressão leva a uma grande simplificação da descrição da atividade neuronal, ultrapassando os resultados de modelos convencionais tais como o de interação entre pares. Como uma generalização, implementamos o nosso modelo de compressão numa população de neurônios do hipocampo, achando de forma geral os mesmos resultados. Isto leva a concluir que a compressão é uma característica geral de redes neuronais de spikes.CNPq - Conselho Nacional de Desenvolvimento Científico e TecnológicoCAPES - Coordenação de Aperfeiçoamento de Pessoal de Nível SuperiorengUniversidade Federal de Minas GeraisPrograma de Pós-Graduação em FísicaUFMGBrasilICX - DEPARTAMENTO DE FÍSICAhttp://creativecommons.org/licenses/by-nc-nd/3.0/pt/info:eu-repo/semantics/openAccessRetinaHipocampoNeuronal codeVisual systemRetinaEfficient codingVertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampusinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/doctoralThesisreponame:Repositório Institucional da UFMGinstname:Universidade Federal de Minas Gerais (UFMG)instacron:UFMGCC-LICENSElicense_rdflicense_rdfapplication/rdf+xml; charset=utf-8811https://repositorio.ufmg.br/bitstream/1843/57796/4/license_rdfcfd6801dba008cb6adbd9838b81582abMD54LICENSElicense.txtlicense.txttext/plain; charset=utf-82118https://repositorio.ufmg.br/bitstream/1843/57796/5/license.txtcda590c95a0b51b4d15f60c9642ca272MD55ORIGINALRamirez_Luisa_Tese.pdfRamirez_Luisa_Tese.pdfapplication/pdf19275619https://repositorio.ufmg.br/bitstream/1843/57796/3/Ramirez_Luisa_Tese.pdf1cf4f130b8127e16c5748ff3e7e2637aMD531843/577962023-08-14 12:46:55.848oai:repositorio.ufmg.br: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ório de PublicaçõesPUBhttps://repositorio.ufmg.br/oaiopendoar:2023-08-14T15:46:55Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)false
dc.title.pt_BR.fl_str_mv Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
title Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
spellingShingle Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
Luisa Fernanda Ramirez Ochoa
Neuronal code
Visual system
Retina
Efficient coding
Retina
Hipocampo
title_short Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
title_full Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
title_fullStr Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
title_full_unstemmed Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
title_sort Vertebrate neuronal networks: efficient coding and compressibility of interactions in the retina and the hippocampus
author Luisa Fernanda Ramirez Ochoa
author_facet Luisa Fernanda Ramirez Ochoa
author_role author
dc.contributor.advisor1.fl_str_mv Ronald Dickman
dc.contributor.advisor1Lattes.fl_str_mv http://lattes.cnpq.br/0484982277336205
dc.contributor.referee1.fl_str_mv William Samuel Bialek
dc.contributor.referee2.fl_str_mv Lucas Lages Wardil
dc.contributor.referee3.fl_str_mv Stephanie Elizabeth Palmer
dc.contributor.referee4.fl_str_mv Mauro Copelli Lopes da Silva
dc.contributor.authorLattes.fl_str_mv http://lattes.cnpq.br/5448393345682958
dc.contributor.author.fl_str_mv Luisa Fernanda Ramirez Ochoa
contributor_str_mv Ronald Dickman
William Samuel Bialek
Lucas Lages Wardil
Stephanie Elizabeth Palmer
Mauro Copelli Lopes da Silva
dc.subject.por.fl_str_mv Neuronal code
Visual system
Retina
Efficient coding
topic Neuronal code
Visual system
Retina
Efficient coding
Retina
Hipocampo
dc.subject.other.pt_BR.fl_str_mv Retina
Hipocampo
description Our success in understanding the retina is partially due to its layered structure, that facilitates the study of circuit motifs and neuronal function. We can understand retinal information processing in three broad stages: I. encoding of light stimuli via electrical signals; II. signal processing by retinal circuits; and III. generation of the retinal code. In this thesis, I focus in the study of the first and third stages from an information-theory perspective. On the first stage, we investigate color coding in zebrafish retinal circuits based on recent experimental findings showing evidence of efficient coding. We propose a theoretical framework to study the encoding performance of different types of outer retinal networks, contrasting the role of excitation and inhibition. More specifically, we use a neuronal population model with chromatic stimulation to study the dynamical properties of such networks. Our findings suggest that inhibition plays a key role in encoding color information reliably, which is not guaranteed in networks with strong excitatory inter-cone couplings. Similarly, we find that networks optimized to encode aquatic spectral information are similar to that observed in zebrafish, providing more general understanding of zebrafish-like retinal circuits of color coding. These results provide quantitative evidence that the zebrafish retina is adapted to efficiently encode information from the environment, enhancing this animal's color vision capabilities. Studies in other species show that animals can adopt different strategies to improve color vision. For instance, in birds and turtles oil droplets serve as a filter to provide a plethora of distinguishable colors. Oil droplets and adapted retinal circuits have been investigated separately. Nevertheless, studies on the combination of both remain unknown. We implement a light transmission model of droplets to investigate the encoding performance of zebrafish-like retinal circuits exhibiting efficient coding. Our findings suggest that introducing droplets in a circuit for chromatic efficient coding creates a trade-off between coding efficiency and color-space gamut. That is, droplets decrease the network encoding performance while increasing the number of distinguishable colors. Regarding the third stage of processing, we focus on the theoretical study of neuronal interactions in the ganglion layer and their compressibility as a path to building simpler models of neuronal activity. Conventional models of neuronal activity introduce assumptions about neural interactions inspired in condensed-matter systems. But these models fail when the number of neurons increases, leading to an exponential explosion in the number of parameters. Here, we implement information theory and renormalization group ideas to explore efficient descriptions of neuronal activity. More specifically, we apply the compression-bottleneck formalism to a population of ganglion cells in the salamander retina. We find that compression leads to a vast simplification in the description of neuronal activity, outperforming conventional pairwise-interaction models. As a generalization, we implement this approach in a population of hippocampus neurons, yielding broadly similar results, suggesting that compressibility is a general feature of spiking neuronal networks.
publishDate 2022
dc.date.issued.fl_str_mv 2022-12-01
dc.date.accessioned.fl_str_mv 2023-08-14T15:46:55Z
dc.date.available.fl_str_mv 2023-08-14T15:46:55Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/doctoralThesis
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dc.identifier.uri.fl_str_mv http://hdl.handle.net/1843/57796
dc.identifier.orcid.pt_BR.fl_str_mv https://orcid.org/0000-0002-8052-3260
url http://hdl.handle.net/1843/57796
https://orcid.org/0000-0002-8052-3260
dc.language.iso.fl_str_mv eng
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dc.publisher.none.fl_str_mv Universidade Federal de Minas Gerais
dc.publisher.program.fl_str_mv Programa de Pós-Graduação em Física
dc.publisher.initials.fl_str_mv UFMG
dc.publisher.country.fl_str_mv Brasil
dc.publisher.department.fl_str_mv ICX - DEPARTAMENTO DE FÍSICA
publisher.none.fl_str_mv Universidade Federal de Minas Gerais
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