Dataset Information

A Neurotransmitter Atlas of the Caenorhabditis elegans Male Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage.

ABSTRACT: The nervous system of most animals is sexually dimorphic but such dimorphisms are generally poorly mapped on an anatomical, cellular, and molecular level. The adult nervous system of the nematode Caenorhabditis elegans displays a number of clearly defined anatomical sexual dimorphisms, but molecular features of sexually dimorphic neurons remain sparse. In this resource paper, we provide a comprehensive atlas of neurotransmitters used in the nervous system of the male and compare it to that of the hermaphrodite. Among the three major neurotransmitter systems, acetylcholine (ACh) is the most frequently used, followed by glutamate (Glu), and lastly ?-aminobutyric acid (GABA). Many male-specific neurons utilize multiple neurotransmitter systems. Interestingly, we find that neurons that are present in both sexes alter their neurotransmitter usage depending on the sex of the animal. One neuron scales up its usage of ACh, another becomes serotonergic in males, and another one adds a new neurotransmitter (glutamate) to its nonsex-specific transmitter (ACh). In all these cases, neurotransmitter changes are correlated with substantial changes in synaptic connectivity. We assembled the neurotransmitter maps of the male-specific nervous system into a comprehensive atlas that describes the anatomical position of all the neurons of the male-specific nervous system relative to the sex-shared nervous system. We exemplify the usefulness of the neurotransmitter atlas by using it as a tool to define the expression pattern of a synaptic organizer molecule in the male tail. Taken together, the male neurotransmitter atlas provides an entry point for future functional and developmental analysis of the male nervous system.

SUBMITTER: Serrano-Saiz E

PROVIDER: S-EPMC5500128 | biostudies-literature | 2017 Jul

REPOSITORIES: biostudies-literature

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A Neurotransmitter Atlas of the <i>Caenorhabditis elegans</i> Male Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage.

Serrano-Saiz Esther E Pereira Laura L Gendrel Marie M Aghayeva Ulkar U Bhattacharya Abhishek A Howell Kelly K Garcia L Rene LR Hobert Oliver O

Genetics 20170701 3

The nervous system of most animals is sexually dimorphic but such dimorphisms are generally poorly mapped on an anatomical, cellular, and molecular level. The adult nervous system of the nematode <i>Caenorhabditis elegans</i> displays a number of clearly defined anatomical sexual dimorphisms, but molecular features of sexually dimorphic neurons remain sparse. In this resource paper, we provide a comprehensive atlas of neurotransmitters used in the nervous system of the male and compare it to tha ...[more]

PMID: 28684604

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Project description:One of the biggest challenges in biology is to understand how activity at the cellular level of neurons, as a result of their mutual interactions, leads to the observed behavior of an organism responding to a variety of environmental stimuli. Investigating the intermediate or mesoscopic level of organization in the nervous system is a vital step towards understanding how the integration of micro-level dynamics results in macro-level functioning. The coordination of many different co-occurring processes at this level underlies the command and control of overall network activity. In this paper, we have considered the somatic nervous system of the nematode Caenorhabditis elegans, for which the entire neuronal connectivity diagram is known. We focus on the organization of the system into modules, i.e., neuronal groups having relatively higher connection density compared to that of the overall network. We show that this mesoscopic feature cannot be explained exclusively in terms of considerations such as, optimizing for resource constraints (viz., total wiring cost) and communication efficiency (i.e., network path length). Even including information about the genetic relatedness of the cells cannot account for the observed modular structure. Comparison with other complex networks designed for efficient transport (of signals or resources) implies that neuronal networks form a distinct class. This suggests that the principal function of the network, viz., processing of sensory information resulting in appropriate motor response, may be playing a vital role in determining the connection topology. Using modular spectral analysis we make explicit the intimate relation between function and structure in the nervous system. This is further brought out by identifying functionally critical neurons purely on the basis of patterns of intra- and inter-modular connections. Our study reveals how the design of the nervous system reflects several constraints, including its key functional role as a processor of information.

Dataset Information

A Neurotransmitter Atlas of the Caenorhabditis elegans Male Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage.

Publications

A Neurotransmitter Atlas of the <i>Caenorhabditis elegans</i> Male Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage.

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