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The role of intensity, temporal synchrony, and biogenic amines for unimodal and multimodal integration during learning and memory of honey bees and bumble bees

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dc.contributor.advisorRiveros Rivera, André Josafat
dc.contributor.gruplacCANNON
dc.creatorGil-Guevara, Oswaldo
dc.creator.degreeDoctor en Ciencias Biomédicas y Biológicas
dc.creator.degreeLevelDoctorado
dc.creator.degreetypeFull time
dc.date.accessioned2024-08-20T12:44:48Z
dc.date.available2024-08-20T12:44:48Z
dc.date.created2023-08-23
dc.date.embargoEndinfo:eu-repo/date/embargoEnd/2025-08-21
dc.descriptionThis PhD thesis investigates the interplay between bimodal signal integration, multisensory processing, and the role of biogenic amines in learning and memory tasks of honey bees and bumble bees. The three chapters provide valuable insights into these interconnected concepts and on the mechanisms underlying bee’s behaviour. The first chapter focuses on the dependency of intensity, for the integration of bimodal signals during learning and memory tasks. My findings demonstrate that successful integration of multimodal signals in honey bees during learning and memory tasks is influenced by the intensity levels of their individual components. This integration follows the principle of inverse effectiveness, akin to observations in vertebrates, suggesting comparable underlying neuronal computations. The second chapter explored the interaction between synchronicity, temporal order and intensity during learning and memory in honey bees. My results support an interaction between the temporal rule and inverse effectiveness principles, suggesting that bees exhibit enhanced perceptual processing when exposed to synchronous bimodal stimuli, particularly at lower levels. Additionally, I found that alternate temporal orders of asynchronous stimuli affected performance only at low intensities. Finally, in chapter 3 I investigated the effects of biogenic amines on unimodal and bimodal PER conditioning in bumble bees expanding our understanding of how octopamine (OA) and dopamine (DA) work in tandem to modulate appetitive learning and memory. My results suggest that the influence of octopamine (OA) and dopamine (DA) administration on learning and memory processes is concentration-dependent and exhibits distinct patterns. Such patterns agree with the well known role of OA as modulator of olfactory and visual learning and including its modulatory role in bimodal learning. While in insects DA is believed to modulate aversive learning here my results suggest an previously unknown inhibitory role during olfactory, visual and bimodal appetitive learning. These results potentially open new avenues of research into the rewarding systems in bees, and insects in general, allowing direct comparisons with vertebrates. Overall, the striking similarities observed between vertebrates and insects regarding multimodal integration principles and the involvement of biogenic amines underscore the universality of these mechanisms across different taxa. These findings contribute to our broader understanding of the neural mechanisms underlying learning and memory processes, emphasizing the adaptive strategies employed by animals in their foraging behaviour involving multiple modalities.
dc.description.abstractMultisensory integration is a fundamental aspect of learning and memory across animals and is particularly relevant during ecological tasks such as foraging and pollination. This study aimed to investigate the influence of external physical properties of unimodal elements of a composed signal such as intensity and the temporal relationships (synchronicity and order) on the multimodal integration of olfactory and visual signals in honey bees. Furthermore, this study targeted the exploration of the impact of biogenic amines on unimodal and multimodal learning and memory processes in bumble bees, recognizing the crucial role of the inner neuromodulatory environment in the formation of rewarding associations. Through an electromechanical setup, bees were trained using precisely controlled intensity levels and temporal relationships (sync /out of sync /alternate orders presentation) of unimodal and bimodal stimuli. The Proboscis Extension Response (PER) conditioning protocol was employed as a measure of reward learning. To manipulate the neuromodulatory environment of bumble bees, oral administration of biogenic amines, octopamine (OA) and dopamine (DA) agonist 6,7-ADTN was employed. Our findings support the Principle of Inverse Effectiveness (PoIE), indicating that bimodal stimuli are more effectively learned and retained when the individual unisensory responses are relatively weak. The interaction between synchrony and intensity significantly influenced bimodal learning and memory, with maximal enhancement observed at low intensities and synchronous stimuli. Furthermore, our investigation into the role of biogenic amines revealed concentration-dependent and opposing effects OA and DA during unimodal and bimodal appetitive learning. Higher doses of OA improved performance across all modalities, while DA had modality and dose-dependent inhibitory effects. These results provide valuable insights into the complex mechanisms and neural modulation underlying appetitive learning tasks in bees, contributing to our understanding of their behavioural adaptation to complex signals. Ultimately, these findings suggest remarkable parallels between the mechanisms of multisensory integration and rewarding systems in bees and vertebrates. These shared characteristics underscore the significance of bees as a valuable comparative model in neuroscience research.
dc.description.sponsorshipPrograma de Becas COLCIENCIAS-Colfuturo No. 727 de la República de Colombia
dc.description.sponsorshipAnimal Behavior Society (ABS Developing Nations Award 2020, otorgado a Oswaldo Gil-Guevara)
dc.format.extent197 pp
dc.format.mimetypeapplication/pdf
dc.identifier.doihttps://doi.org/10.48713/10336_43290
dc.identifier.urihttps://repository.urosario.edu.co/handle/10336/43290
dc.language.isoeng
dc.publisherUniversidad del Rosario
dc.publisher.departmentEscuela de Medicina y Ciencias de la Salud
dc.publisher.programDoctorado en Ciencias Biomédicas y Biológicas
dc.rightsAttribution-NonCommercial-NoDerivatives 4.0 International*
dc.rights.accesRightsinfo:eu-repo/semantics/embargoedAccess
dc.rights.accesoRestringido (Temporalmente bloqueado)
dc.rights.licenciaPARGRAFO: En caso de presentarse cualquier reclamación o acción por parte de un tercero en cuanto a los derechos de autor sobre la obra en cuestión, EL AUTOR, asumirá toda la responsabilidad, y saldrá en defensa de los derechos aquí autorizados; para todos los efectos la universidad actúa como un tercero de buena fe.
dc.rights.urihttp://creativecommons.org/licenses/by-nc-nd/4.0/*
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dc.source.instnameinstname:Universidad del Rosario
dc.source.reponamereponame:Repositorio Institucional EdocUR
dc.subjectIntegracion multimodal
dc.subjectPrincipio de Efectividad Inversa (PoIE)
dc.subjectRegla Temporal de Integración
dc.subjectAminas biogénicas
dc.subjectNeuromodulación
dc.subjectSeñales bimodales
dc.subjectReflejo de extensión de la Proboscide
dc.subjectAprendizaje asociativo
dc.subjectIntegración cros-modal
dc.subjectApis mellifera
dc.subjectBombus impatiens
dc.subjectCondicionamiento absoluto
dc.subjectOrden temporal de los elementos bimodales
dc.subjectCondicionamiento Clásico
dc.subject.keywordMultimodal integration
dc.subject.keywordPrinciple of inverse effectiveness (PoIE)
dc.subject.keywordTemporal rule of integration
dc.subject.keywordTemporal order of bimodal elements
dc.subject.keywordBiogenic amines
dc.subject.keywordNeuromodulation
dc.subject.keywordBimodal signals
dc.subject.keywordProboscis extension reflex (PER)
dc.subject.keywordAssociative learning
dc.subject.keywordCross modal integration
dc.subject.keywordApis mellifera
dc.subject.keywordBombus impatiens
dc.subject.keywordAbsolute conditioning
dc.subject.keywordClassic conditioning
dc.titleThe role of intensity, temporal synchrony, and biogenic amines for unimodal and multimodal integration during learning and memory of honey bees and bumble bees
dc.title.TranslatedTitleEl papel de la intensidad, la sincronía temporal y las aminas biógenas en la integración unimodal y multimodal durante el aprendizaje y la memoria de abejas melíferas y abejorros
dc.typedoctoralThesis
dc.type.documentTesis
dc.type.hasVersioninfo:eu-repo/semantics/acceptedVersion
dc.type.spaTesis de doctorado
local.department.reportEscuela de Medicina y Ciencias de la Salud
local.regionesBogotá
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Doctorado en Ciencias Biomédicas y Biológicas