scholarly journals A collective modulatory basis for multisensory integration in C. elegans

2018 ◽  
Author(s):  
Gareth Harris ◽  
Taihong Wu ◽  
Gaia Linfield ◽  
Myung-Kyu Choi ◽  
He Liu ◽  
...  
Keyword(s):  
Decision Making ◽  
Nervous System ◽  
Multisensory Integration ◽  
Multisensory Processing ◽  
Neurological Diseases ◽  
Sensory Information ◽  
Sensory Cues ◽  
C Elegans ◽  
Behavioral Decision ◽  
Integrated Response

AbstractIn the natural environment, animals often encounter multiple sensory cues that are simultaneously present. The nervous system integrates the relevant sensory information to generate behavioral responses that have adaptive values. However, the signal transduction pathways and the molecules that regulate integrated behavioral response to multiple sensory cues are not well defined. Here, we characterize a collective modulatory basis for a behavioral decision in C. elegans when the animal is presented with an attractive food source together with a repulsive odorant. We show that distributed neuronal components in the worm nervous system and several neuromodulators orchestrate the decision-making process, suggesting that various states and contexts may modulate the multisensory integration. Among these modulators, we identify a new function of a conserved TGF-β pathway that regulates the integrated decision by inhibiting the signaling from a set of central neurons. Interestingly, we find that a common set of modulators, including the TGF-β pathway, regulate the integrated response to the pairing of different foods and repellents. Together, our results provide insights into the modulatory signals regulating multisensory integration and reveal potential mechanistic basis for the complex pathology underlying defects in multisensory processing shared by common neurological diseases.Author SummaryThe present study characterizes the modulation of a behavioral decision in C. elegans when the worm is presented with a food lawn that is paired with a repulsive smell. We show that multiple sensory neurons and interneurons play roles in making the decision. We also identify several modulatory molecules that are essential for the integrated decision when the animal faces a choice between the cues of opposing valence. We further show that many of these factors, which often represent different states and contexts, are common for behavioral decisions that integrate sensory information from different types of foods and repellents. Overall, our results reveal a collective molecular and cellular basis for integration of simultaneously present attractive and repulsive cues to fine-tune decision-making.

scholarly journals Neuroligin dependence of pharyngeal pumping reveals an extrapharyngeal modulation of Caenorhabditis elegans feeding

2018 ◽  
Author(s):  
Fernando Calahorro ◽  
Francesca Keefe ◽  
James Dillon ◽  
Lindy Holden-Dye ◽  
Vincent O’Connor
Keyword(s):  
Decision Making ◽  
Nervous System ◽  
Body Wall ◽  
Neural Circuits ◽  
Orthologous Gene ◽  
Sensory Cues ◽  
C Elegans ◽  
Sensory Modalities ◽  
Pharyngeal Pumping

ABSTRACTThe integration of distinct sensory modalities is essential for behavioural decision making. In C. elegans this process is coordinated by neural circuits that integrate sensory cues from the environment to generate an appropriate behaviour at the appropriate output muscles. Food is a multimodal cue that impacts on the microcircuits to modulating feeding and foraging drivers at the level of the pharyngeal and body wall muscle respectively. When food triggers an upregulation in pharyngeal pumping it allows the effective ingestion of food. Here we show that a C. elegans mutant in the single orthologous gene of human neuroligins, nlg-1 are defective in food induced pumping. This is not explained by an inability to sense food, as nlg-1 mutants are not defective in chemotaxis towards bacteria. In addition, we show that neuroligin is widely expressed in the nervous system including AIY, ADE, ALA, URX and HSN neurones. Interestingly, despite the deficit in pharyngeal pumping neuroligin is not expressed within the pharyngeal neuromuscular network, which suggests an extrapharyngeal regulation of this circuit. We resolve electrophysiologically the neuroligin contribution to the pharyngeal circuit by mimicking a food-dependent pumping, and show that the nlg-1 phenotype is similar to mutants impaired in GABAergic and/or glutamatergic signalling. We suggest that neuroligin organizes extrapharyngeal circuits that regulate the pharynx. These observations based on the molecular and cellular determinants of feeding are consistent with the emerging role of neuroligin in discretely impacting functional circuits underpinning complex behaviours.

scholarly journals Neuropeptides and Behaviors: How Small Peptides Regulate Nervous System Function and Behavioral Outputs

2021 ◽  
Vol 14 ◽  
Author(s):  
Umer Saleem Bhat ◽  
Navneet Shahi ◽  
Siju Surendran ◽  
Kavita Babu
Keyword(s):  
Nervous System ◽  
Behavioral Plasticity ◽  
Environmental Changes ◽  
Sensory Information ◽  
Synaptic Activity ◽  
Small Peptides ◽  
C Elegans ◽  
Wide Range ◽  
Nervous System Function ◽  
Insight Into

One of the reasons that most multicellular animals survive and thrive is because of the adaptable and plastic nature of their nervous systems. For an organism to survive, it is essential for the animal to respond and adapt to environmental changes. This is achieved by sensing external cues and translating them into behaviors through changes in synaptic activity. The nervous system plays a crucial role in constantly evaluating environmental cues and allowing for behavioral plasticity in the organism. Multiple neurotransmitters and neuropeptides have been implicated as key players for integrating sensory information to produce the desired output. Because of its simple nervous system and well-established neuronal connectome, C. elegans acts as an excellent model to understand the mechanisms underlying behavioral plasticity. Here, we critically review how neuropeptides modulate a wide range of behaviors by allowing for changes in neuronal and synaptic signaling. This review will have a specific focus on feeding, mating, sleep, addiction, learning and locomotory behaviors in C. elegans. With a view to understand evolutionary relationships, we explore the functions and associated pathophysiology of C. elegans neuropeptides that are conserved across different phyla. Further, we discuss the mechanisms of neuropeptidergic signaling and how these signals are regulated in different behaviors. Finally, we attempt to provide insight into developing potential therapeutics for neuropeptide-related disorders.

scholarly journals Novel Technological Advances in Functional Connectomics in C. elegans

2019 ◽  
Vol 7 (2) ◽  
pp. 8 ◽  
Author(s):  
DiLoreto ◽  
Chute ◽  
Bryce ◽  
Srinivasan
Keyword(s):  
Nervous System ◽  
Computational Modeling ◽  
Activity Patterns ◽  
Sensory Information ◽  
Neuronal Cell ◽  
Network Models ◽  
Connectivity Matrix ◽  
C Elegans ◽  
Technological Advances

The complete structure and connectivity of the Caenorhabditis elegans nervous system (“mind of a worm”) was first published in 1986, representing a critical milestone in the field of connectomics. The reconstruction of the nervous system (connectome) at the level of synapses provided a unique perspective of understanding how behavior can be coded within the nervous system. The following decades have seen the development of technologies that help understand how neural activity patterns are connected to behavior and modulated by sensory input. Investigations on the developmental origins of the connectome highlight the importance of role of neuronal cell lineages in the final connectivity matrix of the nervous system. Computational modeling of neuronal dynamics not only helps reconstruct the biophysical properties of individual neurons but also allows for subsequent reconstruction of whole-organism neuronal network models. Hence, combining experimental datasets with theoretical modeling of neurons generates a better understanding of organismal behavior. This review discusses some recent technological advances used to analyze and perturb whole-organism neuronal function along with developments in computational modeling, which allows for interrogation of both local and global neural circuits, leading to different behaviors. Combining these approaches will shed light into how neural networks process sensory information to generate the appropriate behavioral output, providing a complete understanding of the worm nervous system.

scholarly journals Concurrent Multisensory Integration and Segregation with Complementary Congruent and Opposite Neurons

2018 ◽  
Author(s):  
Wen-Hao Zhang ◽  
He Wang ◽  
Aihua Chen ◽  
Yong Gu ◽  
Tai Sing Lee ◽  
...  
Keyword(s):  
Multisensory Integration ◽  
Multisensory Processing ◽  
Neural Model ◽  
Cue Integration ◽  
Sensory Cues ◽  
Temporal Area ◽  
Heading Direction ◽  
Vestibular Cues ◽  
The World ◽  
The Brain

Abstract Our brain perceives the world by exploiting multiple sensory modalities to extract information about various aspects of external stimuli. If these sensory cues are from the same stimulus of interest, they should be integrated to improve perception; otherwise, they should be segregated to distinguish different stimuli. In reality, however, the brain faces the challenge of recognizing stimuli without knowing in advance whether sensory cues come from the same or different stimuli. To address this challenge and to recognize stimuli rapidly, we argue that the brain should carry out multisensory integration and segregation concurrently with complementary neuron groups. Studying an example of inferring heading-direction via visual and vestibular cues, we develop a concurrent multisensory processing neural model which consists of two reciprocally connected modules, the dorsal medial superior temporal area (MSTd) and the ventral intraparietal area (VIP), and that at each module, there exists two distinguishing groups of neurons, congruent and opposite neurons. Specifically, congruent neurons implement cue integration, while opposite neurons compute the cue disparity, both optimally as described by Bayesian inference. The two groups of neurons provide complementary information which enables the neural system to assess the validity of cue integration and, if necessary, to recover the lost information associated with individual cues without re-gathering new inputs. Through this process, the brain achieves rapid stimulus perception if the cues come from the same stimulus of interest, and differentiates and recognizes stimuli based on individual cues with little time delay if the cues come from different stimuli of interest. Our study unveils the indispensable role of opposite neurons in multisensory processing and sheds light on our understanding of how the brain achieves multisensory processing efficiently and rapidly.Significance StatementOur brain perceives the world by exploiting multiple sensory cues. These cues need to be integrated to improve perception if they come from the same stimulus and otherwise be segregated. To address the challenge of recognizing whether sensory cues come from the same or different stimuli that are unknown in advance, we propose that the brain should carry out multisensory integration and segregation concurrently with two different neuron groups. Specifically, congruent neurons implement cue integration, while opposite neurons compute the cue disparity, and the interplay between them achieves rapid stimulus recognition without information loss. We apply our model to the example of inferring heading-direction based on visual and vestibular cues and reproduce the experimental data successfully.

Genetics of Behavior in C. elegans

2017 ◽  
pp. 150-170 ◽  
Author(s):  
Denise S. Walker ◽  
Yee Lian Chew ◽  
William R. Schafer
Keyword(s):  
Nervous System ◽  
Caenorhabditis Elegans ◽  
Molecular Genetics ◽  
Sensory Information ◽  
Macro Level ◽  
Gene Products ◽  
Individual Gene ◽  
C Elegans ◽  
Behavioral States ◽  
Motor Outputs

The nematode Caenorhabditis elegans is among the most intensely studied animals in modern experimental biology. In particular, because of its amenability to classical and molecular genetics, its simple and compact nervous system, and its transparency to optogenetic recording and manipulation, C. elegans has been widely used to investigate how individual gene products act in the context of neuronal circuits to generate behavior. C. elegans is the first and at present the only animal whose neuronal connectome has been characterized at the level of individual neurons and synapses, and the wiring of this connectome shows surprising parallels with the micro- and macro-level structures of larger brains. This chapter reviews our current molecular- and circuit-level understanding of behavior in C. elegans. In particular, we discuss mechanisms underlying the processing of sensory information, the generation of specific motor outputs, and the control of behavioral states.

scholarly journals Sexually dimorphic control of gene expression in sensory neurons regulates decision-making behavior in C. elegans

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Zoë A Hilbert ◽  
Dennis H Kim
Keyword(s):  
Gene Expression ◽  
Decision Making ◽  
Sensory Neurons ◽  
Regulation Of Gene Expression ◽  
Sensory Information ◽  
Specific Expression ◽  
Control Of Gene Expression ◽  
Neuron Pair ◽  
C Elegans ◽  
Male Specific

Animal behavior is directed by the integration of sensory information from internal states and the environment. Neuroendocrine regulation of diverse behaviors of Caenorhabditis elegans is under the control of the DAF-7/TGF-β ligand that is secreted from sensory neurons. Here, we show that C. elegans males exhibit an altered, male-specific expression pattern of daf-7 in the ASJ sensory neuron pair with the onset of reproductive maturity, which functions to promote male-specific mate-searching behavior. Molecular genetic analysis of the switch-like regulation of daf-7 expression in the ASJ neuron pair reveals a hierarchy of regulation among multiple inputs—sex, age, nutritional status, and microbial environment—which function in the modulation of behavior. Our results suggest that regulation of gene expression in sensory neurons can function in the integration of a wide array of sensory information and facilitate decision-making behaviors in C. elegans.

scholarly journals The nematode worm C. elegans chooses between bacterial foods exactly as if maximizing economic utility

2021 ◽  
Author(s):  
Abraham Katzen ◽  
Hui-Kuan Chung ◽  
William Harbaugh ◽  
Christina Della Iacono ◽  
Nicholas Jackson ◽  
...  
Keyword(s):  
Decision Making ◽  
Nervous System ◽  
Utility Maximization ◽  
Sufficient Conditions ◽  
Food Choices ◽  
Growth Potential ◽  
C Elegans ◽  
Dopamine Signaling ◽  
Nematode Worm ◽  
As If

In value-based decision making, options are selected according to subjective values assigned by the individual to available goods and actions. Despite the importance of this faculty of the mind, the neural mechanisms of value assignments, and how choices are directed by them, remain obscure. To investigate this problem, we used a classic measure of utility maximization, the Generalized Axiom of Revealed Preference, to quantify internal consistency of food preferences in Caenorhabditis elegans, a nematode worm with a nervous system of only 302 neurons. Using a novel combination of microfluidics and electrophysiology, we found that C. elegans food choices fulfill the necessary and sufficient conditions for utility maximization, indicating that nematodes behave exactly as if they maintain, and attempt to maximize, an underlying representation of subjective value. Food choices are well-fit by a utility function widely used to model human consumers. Moreover, as in many other animals, subjective values in C. elegans are learned, a process we now find requires intact dopamine signaling. Differential responses of identified chemosensory neurons to foods with distinct growth potential are amplified by prior consumption of these foods, suggesting that these neurons may be part of a value-assignment system. The demonstration of utility maximization in an organism with a nervous system of only 302 neurons sets a new lower bound on the computational requirements for its execution, and offers the prospect of an essentially complete explanation of value-based decision making at single neuron resolution.

scholarly journals Calcium dynamics regulating the timing of decision-making in C. elegans

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Yuki Tanimoto ◽  
Akiko Yamazoe-Umemoto ◽  
Kosuke Fujita ◽  
Yuya Kawazoe ◽  
Yosuke Miyanishi ◽  
...  
Keyword(s):  
Decision Making ◽  
Calcium Channels ◽  
Molecular Mechanisms ◽  
Neuronal Responses ◽  
Odor Concentration ◽  
Nociceptive Neurons ◽  
C Elegans ◽  
Behavioral Decision ◽  
Voltage Gated Calcium Channels ◽  
Multiple Trials

Brains regulate behavioral responses with distinct timings. Here we investigate the cellular and molecular mechanisms underlying the timing of decision-making during olfactory navigation in Caenorhabditis elegans. We find that, based on subtle changes in odor concentrations, the animals appear to choose the appropriate migratory direction from multiple trials as a form of behavioral decision-making. Through optophysiological, mathematical and genetic analyses of neural activity under virtual odor gradients, we further find that odor concentration information is temporally integrated for a decision by a gradual increase in intracellular calcium concentration ([Ca2+]i), which occurs via L-type voltage-gated calcium channels in a pair of olfactory neurons. In contrast, for a reflex-like behavioral response, [Ca2+]i rapidly increases via multiple types of calcium channels in a pair of nociceptive neurons. Thus, the timing of neuronal responses is determined by cell type-dependent involvement of calcium channels, which may serve as a cellular basis for decision-making.

scholarly journals The interplay between multisensory integration and perceptual decision making

2019 ◽  
Author(s):  
Manuel R. Mercier ◽  
Celine Cappe
Keyword(s):  
Decision Making ◽  
Multisensory Integration ◽  
Multisensory Processing ◽  
Optimal Decision ◽  
Perceptual Decision Making ◽  
Perceptual Decision ◽  
Human Participants ◽  
Sensory Encoding ◽  
Optimal Decision Making ◽  
The Brain

AbstractFacing perceptual uncertainty, the brain combines information from different senses to shape optimal decision making and to guide behavior. Despite overlapping neural networks underlying multisensory integration and perceptual decision making, the process chain of decision formation has been studied mostly in unimodal contexts and is thought to be supramodal. To reveal whether and how multisensory processing interplay with perceptual decision making, we devised a paradigm mimicking naturalistic situations where human participants were exposed to continuous cacophonous audiovisual inputs containing an unpredictable relevant signal cue in one or two modalities. Using multivariate pattern analysis on concurrently recorded EEG, we decoded the neural signatures of sensory encoding and decision formation stages. Generalization analyses across conditions and time revealed that multisensory signal cues were processed faster during both processing stages. We further established that acceleration of neural dynamics was directly linked to two distinct multisensory integration processes and associated with multisensory benefit. Our results, substantiated in both detection and categorization tasks, provide evidence that the brain integrates signals from different modalities at both the sensory encoding and the decision formation stages.

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