Exploring the Neural Basis of Chemosensory Behaviors in Caenorhabditis Elegans: How Context and Experience Shape Sensory Perception

Exploring the Neural Basis of Chemosensory Behaviors in Caenorhabditis Elegans: How Context and Experience Shape Sensory Perception PDF Author: Manon Guillermin
Publisher:
ISBN:
Category :
Languages : en
Pages : 97

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Book Description
Adaptability is essential to organisms' fitness and survival. Evolutionary success depends on access to an array of behavioral choices in the face of changing environmental conditions. To navigate complex landscapes, organisms can interpret the significance of sensory stimuli, and assign context-appropriate valence, by integrating factors such as cues from their internal and external environments, and memories of previously experienced conditions, to dynamically shape neural circuits and generate ethologically relevant behaviors. In this thesis, I explore the cellular and molecular mechanisms that shape the carbon dioxide (CO2) circuit in the free-living nematode, Caenorhabditis elegans. CO2 is a complex sensory cue that can signify the presence of fruitful or dangerous surroundings. As a result, C. elegans can display a variety of different behaviors in response to CO2, from robust attraction to robust avoidance. Although sensory signaling of the CO2-responsive BAG neurons has been extensively characterized, how BAG communicates with postsynaptic interneurons, and how the CO2 signal is propagated through the nervous system to generate a context-appropriate behavior is unknown. First, we have found that neuromodulatory state and environmental oxygen (O2) levels converge on the CO2 circuit via the URX sensory neurons. The lab-derived N2 C. elegans strain expresses high levels of NPR-1 neuropeptide receptor, which inhibits URX and results in CO2 avoidance, regardless of environmental O2. In the C. elegans wild isolate "Hawaii", loss of npr-1 leads to modulation of URX by environmental O2, and results in CO2 avoidance at low O2, and loss of CO2-evoked behavior at high O2. Second, we present a new circuit motif that demonstrates how divergent responses to a single sensory input, CO2, can arise from an identical set of sensory and interneuron connections. We show that C. elegans exhibit an experience-dependent behavioral valence switch in response to CO2. While animals raised at ambient CO2 are repelled by CO2, animals raised in a high CO2 environment are attracted to CO2. Whether CO2 is attractive or repulsive is determined by the coordinated activity of specialized valence-encoding interneurons, AIY, RIG, and RIA, whose responses are subject to context-dependent modulation. An additional interneuron pair, AIZ, regulates behavioral sensitivity regardless of valence. Glutamatergic and neuropeptidergic signaling mediate both CO2 avoidance and attraction, and different neuropeptides play distinct roles in regulating valence and sensitivity. Our results elucidate a microcircuit motif whereby a fixed set of neurons are leveraged to generate alternative outputs in response to a single chemosensory input.

Exploring the Neural Basis of Chemosensory Behaviors in Caenorhabditis Elegans: How Context and Experience Shape Sensory Perception

Exploring the Neural Basis of Chemosensory Behaviors in Caenorhabditis Elegans: How Context and Experience Shape Sensory Perception PDF Author: Manon Guillermin
Publisher:
ISBN:
Category :
Languages : en
Pages : 97

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Book Description
Adaptability is essential to organisms' fitness and survival. Evolutionary success depends on access to an array of behavioral choices in the face of changing environmental conditions. To navigate complex landscapes, organisms can interpret the significance of sensory stimuli, and assign context-appropriate valence, by integrating factors such as cues from their internal and external environments, and memories of previously experienced conditions, to dynamically shape neural circuits and generate ethologically relevant behaviors. In this thesis, I explore the cellular and molecular mechanisms that shape the carbon dioxide (CO2) circuit in the free-living nematode, Caenorhabditis elegans. CO2 is a complex sensory cue that can signify the presence of fruitful or dangerous surroundings. As a result, C. elegans can display a variety of different behaviors in response to CO2, from robust attraction to robust avoidance. Although sensory signaling of the CO2-responsive BAG neurons has been extensively characterized, how BAG communicates with postsynaptic interneurons, and how the CO2 signal is propagated through the nervous system to generate a context-appropriate behavior is unknown. First, we have found that neuromodulatory state and environmental oxygen (O2) levels converge on the CO2 circuit via the URX sensory neurons. The lab-derived N2 C. elegans strain expresses high levels of NPR-1 neuropeptide receptor, which inhibits URX and results in CO2 avoidance, regardless of environmental O2. In the C. elegans wild isolate "Hawaii", loss of npr-1 leads to modulation of URX by environmental O2, and results in CO2 avoidance at low O2, and loss of CO2-evoked behavior at high O2. Second, we present a new circuit motif that demonstrates how divergent responses to a single sensory input, CO2, can arise from an identical set of sensory and interneuron connections. We show that C. elegans exhibit an experience-dependent behavioral valence switch in response to CO2. While animals raised at ambient CO2 are repelled by CO2, animals raised in a high CO2 environment are attracted to CO2. Whether CO2 is attractive or repulsive is determined by the coordinated activity of specialized valence-encoding interneurons, AIY, RIG, and RIA, whose responses are subject to context-dependent modulation. An additional interneuron pair, AIZ, regulates behavioral sensitivity regardless of valence. Glutamatergic and neuropeptidergic signaling mediate both CO2 avoidance and attraction, and different neuropeptides play distinct roles in regulating valence and sensitivity. Our results elucidate a microcircuit motif whereby a fixed set of neurons are leveraged to generate alternative outputs in response to a single chemosensory input.

Neurotransmission Defines Functional Chemosensory Neural Circuits to Regulate Behavior

Neurotransmission Defines Functional Chemosensory Neural Circuits to Regulate Behavior PDF Author: Sarah Goldberg Leinwand
Publisher:
ISBN: 9781321870589
Category :
Languages : en
Pages : 157

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Book Description
Neural circuits detect and process environmental changes to drive appropriate food-seeking or toxin-avoiding behaviors. However, we lack a complete understanding of the cellular and molecular mechanisms that represent chemosensory cues and generate appropriate behaviors. Furthermore, these vital sensory abilities deteriorate with age in humans and most animals, but it is unknown how aging impairs the underlying neural circuits to cause sensory behavioral declines. With powerful genetic tools, a complete connectome and robust chemosensory behaviors, the nematode Caenorhabditis elegans is ideally suited for a circuit-level analysis of these behaviors in young and aged animals. The aim of this dissertation is to identify neural signaling and circuit principles for flexibly encoding chemosensory stimuli and generating behavioral plasticity in C. elegans, which may be broadly conserved. In Chapters 2 and 3, I define a novel, sensory context-dependent and neuropeptide-regulated switch in the composition of a C. elegans salt sensory circuit. The ASE primary salt sensory neurons cleave and release insulin-like peptides in response to large but not small changes in external salt stimuli. Insulin signaling functionally switches the AWC olfactory sensory neuron into an interneuron in the high salt circuit, potentiating behavioral responses. Thus, sensory context and neuropeptide signaling act together to shape the flow of information in active neural circuits, suggesting a general mechanism for generating dynamic behavioral outputs. In Chapter 4, I identify an aging-associated decline in C. elegans olfactory behavior and map a novel underlying circuit motif. Two primary olfactory sensory neuron pairs, AWC and AWA, directly detect benzaldehyde and release insulin peptides and acetylcholine to activate two secondary neuron pairs, ASE and AWB, and drive behavioral plasticity. Interestingly, odor-evoked activity in the secondary, but not primary, neurons degrades with age. Experimental manipulations to increase primary neuron transmitter release rescue these aging-associated neuronal deficits. Furthermore, aged animals' olfactory abilities are correlated with lifespan, suggesting that olfaction may be indicative of overall health and physiology. These results show how chemosensory stimuli are encoded by a population code composed of primary and secondary neurons and suggest reduced neurotransmission as a novel mechanism driving aging-associated sensory neural activity and behavioral declines. In sum, this dissertation establishes the crucial role of peptidergic and classical neurotransmission in defining the active neural circuit configurations that regulate chemosensory behaviors.

The Neurobiology of C. elegans

The Neurobiology of C. elegans PDF Author:
Publisher: Elsevier
ISBN: 0080478611
Category : Medical
Languages : en
Pages : 242

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Book Description
The Neurobiology of C. elegans assembles together a series of chapters describing the progress researchers have made toward solving some of the major problems in neurobiology with the use of this powerful model organism. The first chapter is an introduction to the anatomy of the C. elegans nervous system. This chapter provides a useful introduction to this system and will help the reader who is less familiar with this system understand the chapters that follow. The next two chapters on learning, conditioning and memory and neuronal specification and differentiation, summarize the current state of the C. elegans field in these two major areas of neurobiology. The remaining chapters describe studies in C. elegans that have provided particularly exciting insights into neurobiology.

Bottom-up and Top-down: Molecules and Circuits that Underlie Chemosensory Behaviors

Bottom-up and Top-down: Molecules and Circuits that Underlie Chemosensory Behaviors PDF Author: Markus Rothermel
Publisher: Frontiers Media SA
ISBN: 288971442X
Category : Science
Languages : en
Pages : 133

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Book Description


Invertebrate Learning and Memory

Invertebrate Learning and Memory PDF Author: Andrea H. McEwan
Publisher: Elsevier Inc. Chapters
ISBN: 0128071575
Category : Medical
Languages : en
Pages : 53

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Book Description
Despite its apparent simplicity, the soil-dwelling nematode Caenorhabditis elegans has a surprisingly large capacity to learn and remember. Previous characterization of C. elegans genome and neuronal circuit makes this worm an ideal choice for studying behavior and the mechanisms that underlie it. Through careful behavioral and genetic studies, nematodes have been shown to form both short-term and long-term memory in associative and nonassociative training paradigms. Investigations of mechanosensory habituation and context-dependent learning in C. elegans have uncovered important similarities between learning in C. elegans and learning in vertebrates. These results include the discovery of common behavioral features in nonassociative learning between C. elegans and other organisms along with the identification of conserved genes that govern both nonassociative and associative learning. High-throughput studies have identified hundreds of genes implicated in memory and will potentially lead to insights into the fundamental strategies for encoding memory.

C. Elegans Behaviors and Their Mechanosensory Drivers

C. Elegans Behaviors and Their Mechanosensory Drivers PDF Author: Mochi Liu
Publisher:
ISBN:
Category :
Languages : en
Pages : 0

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Book Description
One of the fundamental problems in neuroscience is how behavior is generated from sensory input and internal neural states, such as the animal?s behavioral context. We present new methods and findings to address this by studying the model organism Caenorhabditis elegans. With a fully mapped connectome of 302 neurons, this nematode is a particularly good candidate to investigate the neural basis of behavior due to its rich history of scientific research and its optical transparency. First, we showcase an instrument that can record panneuronal calcium activity in the head of a freely moving worm at single neuron resolution. We find multiple neurons have correlated activity with behaviors such as forward, backward, and turning locomotion. We also developed a high-throughput method to measure sensorimotor transformations from soft touch stimulation to locomotory behavior. We use automated behavior segmentation and reverse correlation to reveal how mechanosensory stimuli influences behavioral transitions. Our results show that C. elegans make locomotory decisions based on both the temporal history of the stimulus and its own behavioral context in a predictable manner. Continuing our investigation of the soft touch circuit, we developed a more advanced apparatus that can probe worm behavioral response to excitatory and inhibitory optogenetic stimuli with sub-animal level spatial resolution. This instrument has the ability to target the heads and tails of many animals in parallel, and can tailor the stimuli based on real-time behavior information. Preliminary experiments demonstrate that it can evoke the same optogenetically driven touch response akin to mechanical activation of the touch neurons.

Molecular Genetic Analysis of Chemosensory Behaviors in C. Elegans

Molecular Genetic Analysis of Chemosensory Behaviors in C. Elegans PDF Author: Joseph H. Chou
Publisher:
ISBN:
Category : Caenorhabditis elegans
Languages : en
Pages : 362

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Book Description


Invertebrate Learning and Memory

Invertebrate Learning and Memory PDF Author: Hiroyuki Sasakura
Publisher: Elsevier Inc. Chapters
ISBN: 0128071591
Category : Medical
Languages : en
Pages : 41

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Book Description
Thermotaxis of the nematode Caenorhabditis elegans is a suitable behavior for the study of neural plasticity. The simple neural circuit for thermotaxis provides the guideline for information processing. Recently developed techniques for optically manipulating neuronal activity and neural imaging have facilitated the dissection of such neural processing. Thermosensory neurons remember sensed temperatures. Part of highly sophisticated and complicated information flow between sensory neurons and interneurons has also been revealed. Recent finding have revealed that evolutionally conserved molecules such as insulin, monoamines, and neuropeptides are required for the plasticity. We propose the functional analogy between the thermotaxis neural circuit and human brain structure, which may help elucidation of the in-depth circuit operation of human brain.

Olfactory memory networks: from emotional learning to social behaviors

Olfactory memory networks: from emotional learning to social behaviors PDF Author: Regina M. Sullivan
Publisher: Frontiers Media SA
ISBN: 2889194868
Category : Brain
Languages : en
Pages : 289

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Book Description
Odors are powerful stimuli that can evoke emotional states, and support learning and memory. Decades of research have indicated that the neural basis for this strong “odor-emotional memory” connection is due to the uniqueness of the anatomy of the olfactory pathways. Indeed, unlike the other sensory systems, the sense of smell does not pass through the thalamus to be routed to the cortex. Rather, odor information is relayed directly to the limbic system, a brain region typically associated with memory and emotional processes. This provides olfaction with a unique and potent power to influence mood, acquisition of new information, and use of information in many different contexts including social interactions. Indeed, olfaction is crucially involved in behaviors essential for survival of the individual and species, including identification of predators, recognition of individuals for procreation or social hierarchy, location of food, as well as attachment between mating pairs and infant-caretaker dyads. Importantly, odors are sampled through sniffing behavior. This active sensing plays an important role in exploratory behaviors observed in the different contexts mentioned above. Odors are also critical for learning and memory about events and places and constitute efficient retrieval cues for the recall of emotional episodic memories. This broad role for odors appears highly preserved across species. In addition, the consistent early developmental emergence of olfactory function across diverse species also provides a unique window of opportunity for analysis of myriad behavioral systems from rodents to nonhuman primates and humans. This, when combined with the relatively conserved organization of the olfactory system in mammals, provides a powerful framework to explore how complex behaviors can be modulated by odors to produce adaptive responses, and to investigate the underlying neural networks. The present research topic brings together cutting edge research on diverse species and developmental stages, highlighting convergence and divergence between humans and animals to facilitate translational research.

The Neurobiology of Olfaction

The Neurobiology of Olfaction PDF Author: Anna Menini
Publisher: CRC Press
ISBN: 1420071998
Category : Science
Languages : en
Pages : 438

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Book Description
Comprehensive Overview of Advances in OlfactionThe common belief is that human smell perception is much reduced compared with other mammals, so that whatever abilities are uncovered and investigated in animal research would have little significance for humans. However, new evidence from a variety of sources indicates this traditional view is likely