Analysis of information processing in the olfactory bulb by in vivo experiments and theoretical modelling

Brice Bathellier
EPFL, 2007
Thèse EPFL

Résumé

Much information is conveyed to animals by the diverse molecules propagated in their environment. This information is transmitted and treated within the olfactory system to be utilized by the rest of the brain. In this process, the sensory flow arriving from the nose first encounters the olfactory bulb. This thesis studies different aspects of the encoding and treatment of olfactory information in the bulb by a combination of experimental and theoretical approaches. The olfactory bulb consists of two functional stages: an input stage where the nerve terminals from the sensory neurons of the nose are spatially arranged in a precise manner, and an output stage corresponding to the neurons which propagate the processed information towards the more central brain areas. The first part of this thesis is focused on the development of an image processing technique to precisely map the input stage. In a second part, output neurons activity in responsive areas of the bulb was recorded in anaesthetized mice. The data obtained indicate complex dynamics in neural activity on several time scales. We show that the combination of mean firing rates from a large enough ensemble of neurons allows to accurately predict the odor presented to the animal. We also show that temporal variables related to the dynamics give very little information complementary to the ensemble rate code, suggesting that these variables are not read by brain structures downstream to the bulb. In a third part, we developed a numerical model of the olfactory bulb to understand its fast oscillatory dynamics. The model proposes a mechanism based on the negative feedback from the interneurons that regulate output neurons. Some predictions of the model are checked experimentally. An analytical interpretation of the model is also proposed and its generalization to the analysis of fast oscillation in other parts of the brain is discussed.

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https://infoscience.epfl.ch/record/109930?ln=fr

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Brice Bathellier
EPFL, 2007
Thèse EPFL

Résumé

Official source

https://infoscience.epfl.ch/record/109930?ln=fr

À propos de ce résultat

Concepts associés (25)

vignette|Cerveau d'un chimpanzé. Le cerveau est le principal organe du système nerveux des animaux bilatériens. Ce terme tient du langage courant (non scientifique) et chez les chordés, comme les hum

Le bulbe olfactif (BO), parfois appelé lobe olfactif, est une région du cerveau des vertébrés dont la fonction principale est de traiter les informations olfactives en provenance des neurones chémor

Un rythme cérébral (appelé aussi activité neuro-électrique) désigne l'oscillation électromagnétique émise par le cerveau des êtres humains, mais également de tout être vivant. Le cortex frontal qui

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Uncovering the neural encoding of behavior in the adult Drosophila motor system

Chin-Lin Chen

One of the most important goals in neuroscience research has always been to understand how animals control their behavior. However, the long focus on the role of brain neurons in behavioral control might be missing the full story. In fact, brain-wide fluctuations in neural activity are highly correlated to the behavioral state, suggesting a closed-loop system where the behavioral command and the body state interact to interpret sensory inputs and dynamically guide action selection. However, to date, little is known about how and where information about the behavioral state is generated. In principle, information about the behavioral state is a relatively high-level encoding of the body state derived from the integration of signals from primary sensors and the local network. Local motor circuits residing in the spinal cord of mammals or the ventral nerve cord (VNC) of insects may give rise to the behavioral state and pass to the brain via brain-projecting interneurons---termed ascending neurons (ANs). However, what information ANs carry and where this information originates is still a mystery due to the technical challenges in measuring these signals in behaving animals. Therefore, it is critical to develop tools to track neuron identity and record neuronal activity during behavior to crack the functional network. In this work, a method is introduced for imaging the motor circuit in the VNC of Drosophila melanogaster. This preparation demonstrates how to retain fly limb function after dissection and allows simultaneous recording of a tethered fly's behavior and its neural activity in the VNC. Incorporating this methodology with other approaches can verify the conclusions from the experiments such as those manipulating neuronal excitability, and motivate further investigation into neuronal function in specific types of behavior. Since it has long been theorized that ANs are the cellular basis of the behavioral state information sent in the brain, the technique introduced in this work was designed to resolve questions relating to what type of information ANs convey. Here, a large-scale functional screen was performed to relate neural activity, behavior, and neuronal morphology for 247 genetically identified ANs in the adult fly. This is the first large-scale screen of neural activity in a behaving animal, and this work uncovered three fundamental features of AN populations. First, rather than low-level limb movements, ANs encode high-level behaviors like walking, grooming, and resting. Second, ANs project nearly exclusively to an integrative sensory center (AVLP) and an action selection hub (GNG). Remarkably, the encodings projected to these distinct areas reflect their potential roles in contextualizing sensory cues (AVLP) and guiding future actions (GNG). Third, the behavioral encodings of ANs are closely linked to their motor system patterning. In conclusion, this work provides an indispensable tool to study the motor system beyond the brain network by overcoming a major technical barrier in in-vivo recording of the VNC of a behaving fly. This tool was used to help resolve what is encoded by ANs as a higher-level behavioral state, suggesting that the primary cellular origin of the behavioral information that is used to modulate brain function comes from the VNC. Overall, the technique and the findings on AN encoding should inspire follow-up studies to uncover additional neural mechanisms used in adaptive behavior generation.

EPFL2022

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Cellular mechanisms regulating adult neurogenesis and olfactory perception in mice

Thomas Brionne, Maria del Carmen Sandi Perez

In the adult mammalian brain, neural stem cells persist in the subventricular zone and the hippocampus, producing new functional neurons throughout life. Whether and how adult neurogenesis maintains brain function remains highly debated. This question is of primary interest due to the potential therapeutic use of adult neurogenesis in treating neurodegenerative disease. Furthermore, understanding the functional impact of adult neurogenesis on the sense of smell may help deciphering the neural code underlying odor recognition. In this thesis work, we impaired adult neurogenesis using molecular, transgenic and focal irradiation approaches. We assessed olfactory function using in vitro and in vivo electrophysiology, in vivo optical imaging and behavioral psychophysical measurements. We show that reducing the number of newborn interneurons decreases the level of synchronized firing of the projection neurons and leads to impaired olfactory discrimination performance in behaving mice. By isolation of specific olfactory bulb cellular populations, we provide a series of genetic markers differentiating newborn cells from mature neurons that mediate the observed function of olfactory neurogenesis. This thesis work demonstrates that adult neurogenesis represents a new form of plasticity that supports brain function, controlling olfactory information processing already at the first central relay. Finally our data give also insights about the cellular and molecular mechanisms occurring in the olfactory bulb network controlling sensory perception, and help define key genes in the neuronal maturation process.

EPFL2007

Chargement

Understanding how neural circuits remodel and adapt to animal behavior is a central theme in the field of Neuroscience. One strategy to reach this goal is to repeatedly record the same animal's neural circuits and observe how they adapt when facing different challenges. Research has primarily focused on identifying neural circuits and connectivity maps within the brains of model organisms. Nevertheless, it has become evident that functional recordings are essential to have a complete understanding of how neural circuits generate behaviors. Numerous techniques have been introduced to record activity from brain circuits in model animals spanning from monkeys to insects. However, imaging the spinal cord in mammals or the ventral nerve cord in insects remains an open challenge due to the complexity of obtaining optical access without impacting the animal's behavior and damaging neural tissues. As a result, we have very limited information on how neural circuits in the spinal cord generate behaviors and how they adapt to different experiences such as injury or aging. Drosophila is a perfect model organism for carrying out this line of research thanks to its small size, genetically tractable nervous system, and behavioral diversity. The results are relevant to human physiology and behavior as many mechanisms have homologs in mammals. What is missing is a technological advancement that allows recording of behavior, structural changes in the circuits, and spatiotemporal dynamics of neural activity on the same animal.This thesis addresses this gap and introduces two novel methods for in vivo functional recordings of the fly's ventral nerve cord (VNC). The first one gains short-term access to the fly's VNC using a novel dissection preparation. The second one enables long-term functional recordings of the fly's VNC thanks to a toolkit combining four microengineered devices: a surgical arm, a V-shape implant, an optically transparent and numbered window and a remounting stage. The toolkit is suitable for both male and female flies and provides optical access to the VNC for at least one month. Additionally, the long-term toolkit does not impact flies' behaviors compared to intact flies and can be used to image both sparse and large populations of neural activity in flies' cervical connective and VNC. The toolkit was tested in two proof-of-concept (POC) applications. In the first POC, the toolkit monitored the degradation of sensory neurons in the VNC over weeks following limb amputation. In the second POC, the toolkit monitored global changes in neural dynamics following ingestion of a high-concentration caffeine solution. In conclusion, this thesis introduces new techniques for functional recordings of the fly's cervical connective and VNC over short and long time scales. They enable optical access to the fly's cervical connective that can be leveraged to study the content of information transmitted between the brain and the VNC while the fly is behaving. The two POCs demonstrate that the novel technology is ideally suited for long-term experiments and could be applied to a wide range of studies. For instance, the toolkit could be used to investigate how behaviors are encoded in the fly's VNC and how they adapt over time to experiences such as disease, aging, drug intake and learning.

EPFL2022

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Uncovering the neural encoding of behavior in the adult Drosophila motor system

Chin-Lin Chen

EPFL2022