Nematode Neurons: Anatomy and Anatomical Methods in Caenorhabditis elegans

David H. Hall, Robyn Lints, Zeynep Altun

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

The nematode nervous system is less centralized than those in higher animals (Bullock and Horridge, 1965), although the nerve ring in the head does bring together the majority of the body's neurons and synapses. The adult male also has enlarged tail ganglia (gaining 89 extra neurons) that function as a major processing center in the tail to control aspects of male mating behavior (discussed in Chapter 4). The largest proportion of synaptic neuropil is consolidated in the nerve ring itself. There is no separate neuropil associated with most clusters (ganglia) of cell bodies that surround the ring (Table I). Aside from the nerve ring and its extension beneath the nearby retrovesicular ganglion, the other principal sites of synaptic interactions consist of the ventral and dorsal nerve cords (discussed in Chapter 5) and in the preanal ganglion in the tail (Hall and Russell, 1991). A limited synaptic zone is associated with the egg-laying system at the vulva (Thomas et al., 1990). Synapses in other peripheral locales are rare. The nematode was the first eukaryote in which all neuronal and glial cell fates could be identified and characterized. The comprehensive nature of our knowledge of physical, molecular, and developmental aspects of these cells potentiates C. elegans as a model system for exploring both the development and function of complete behavioral circuits as well as the genetic specification of neuronal characters in isolation. Similarities between nematode neurons and those in other organisms include the early guidance receptors used for axon outgrowth, and the cellular machinery (e.g., vesicular transporters, ion channels, synaptic proteins) utilized to carry out mature functions (Ruvkun and Hobert, 1998) (see Chapter 3). The ligands used for cell signaling and the transmitters (both classical neurotransmitters [such as GABA, acetylcholine, serotonin, and so on] and neuropeptides) used in neuronal signaling are generally conserved as well (Bargmann, 1998) (see Chapter 3). Classification of nematode neurons into functional categories was initially done according to transmission electron microscopy (TEM) data alone (Albertson and Thomson, 1976; Hall, 1977; Sulston et al., 1980; Ward et al., 1975; Ware et al., 1975; White et al., 1976, 1986). Motor neurons comprised all of those cells that consistently formed neuromuscular junctions (NMJs) onto one or more muscle cells. Sensory neurons were those cells that possessed a distinct sensory dendrite of any modality (although the specific modality often awaited physiological testing, laser ablation, or mutant behavior). Interneurons comprised most of the rest; where their synaptic wiring imputed some role in collecting and relaying synaptic activity from upstream (sensory or interneuron) neurons to downstream effector neurons. Some neurons that have been categorized as "sensory" or "motor" cells may also have a high degree of interconnectivity that would also classify them as interneurons. Some neurons displayed dual roles ("polymodal"), for instance having both a sensory dendrite and NMJ outputs. Several neurons with few distinctive features were difficult to categorize. Anatomic and genetic studies have identified several "pioneer neurons" that play important roles in axon guidance or maintenance, while having little or no role in synaptic circuits (Aurelio et al., 2002; Chen et al., 2005; Durbin, 1987; Wadsworth et al., 1996). Some potential neurons undergo early apoptotic deaths soon after their birth and could not be categorized into a functional class (Sulston et al., 1983). Some neurons change their principal wiring features during development, adding new synapses and deleting others (Walthall, 1990; White et al., 1978). Evidence is less solid regarding whether nematode neurons can modify their circuitry in response to the animal's experience, although their patterns of activity must surely vary according to this experience (Chao et al., 2004; Gomez et al., 2001; Peckol et al., 1999, 2001; Zhao and Nonet, 2000) (see Chapter 2). Regions important for sensory transduction in a nematode neuron are not always identifiable by their TEM structure alone, and thus certain cells evade easy categorization. For these reasons, the final tabulation of neuron subclasses has required occasional corrections as more physiological and developmental data has accumulated. The basic structure of a C. elegans neuron consists of a monopolar or bipolar cell extending one or two simple thin processes (neurites) along the length of the body (Fig. 1). The cell body is generally about 2 μm in diameter and contains a small compact nucleus. The neurites are extremely narrow in diameter (often just ≤0.2 μm) and most have virtually no local branches. Since the typical neuron is essentially unbranched, it must send its neurite along a local "neighborhood" in close proximity with its chosen partners before forming many synapses (White et al., 1983). Synapses occur en passant at local swellings along the length of a neurite (Fig. 2). A neurite often ends by making a gap junction (electrical synapse) where it contacts the neurite of a homologous neuron, such that neither cell extends a process into a territory occupied by its homologues (thus, the axon of VD4 will form junctions at its anterior and posterior limits with the axons of VD3 and VD5 in the ventral cord, and axons of left/right neuron pairs often form junctions where they meet in the nerve ring). Thus, the nervous system is exceedingly economical not only in cell number but also in the number of processes or branches. Even the final positions of neuron cell bodies seem efficiently managed to minimize the total "wiring cost" of the nervous system (Chen et al., 2005). The total number of synapses per neuron is also remarkably limited. The hermaphrodite adult contains about 5000 chemical synapses, 700 gap junctions and 2000 NMJs. Many cells only form 25 to 50 synapses, and certain neurons form fewer than 10 synapses in total, including repeated contacts to the same partner. Even the most important command interneurons have about 200 synapses in total.

Original languageEnglish (US)
Pages (from-to)1-35
Number of pages35
JournalInternational Review of Neurobiology
Volume69
DOIs
StatePublished - 2005

Fingerprint

Caenorhabditis elegans
Anatomy
Neurons
Synapses
Neurites
Interneurons
Ganglia
Neuromuscular Junction
Nervous System
Axons
Tail
Neuropil
Gap Junctions
Dendrites
Transmission Electron Microscopy
Electrical Synapses

ASJC Scopus subject areas

  • Neuroscience(all)
  • Neuropsychology and Physiological Psychology
  • Physiology

Cite this

Nematode Neurons : Anatomy and Anatomical Methods in Caenorhabditis elegans. / Hall, David H.; Lints, Robyn; Altun, Zeynep.

In: International Review of Neurobiology, Vol. 69, 2005, p. 1-35.

Research output: Contribution to journalArticle

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A limited synaptic zone is associated with the egg-laying system at the vulva (Thomas et al., 1990). Synapses in other peripheral locales are rare. The nematode was the first eukaryote in which all neuronal and glial cell fates could be identified and characterized. The comprehensive nature of our knowledge of physical, molecular, and developmental aspects of these cells potentiates C. elegans as a model system for exploring both the development and function of complete behavioral circuits as well as the genetic specification of neuronal characters in isolation. Similarities between nematode neurons and those in other organisms include the early guidance receptors used for axon outgrowth, and the cellular machinery (e.g., vesicular transporters, ion channels, synaptic proteins) utilized to carry out mature functions (Ruvkun and Hobert, 1998) (see Chapter 3). The ligands used for cell signaling and the transmitters (both classical neurotransmitters [such as GABA, acetylcholine, serotonin, and so on] and neuropeptides) used in neuronal signaling are generally conserved as well (Bargmann, 1998) (see Chapter 3). Classification of nematode neurons into functional categories was initially done according to transmission electron microscopy (TEM) data alone (Albertson and Thomson, 1976; Hall, 1977; Sulston et al., 1980; Ward et al., 1975; Ware et al., 1975; White et al., 1976, 1986). Motor neurons comprised all of those cells that consistently formed neuromuscular junctions (NMJs) onto one or more muscle cells. Sensory neurons were those cells that possessed a distinct sensory dendrite of any modality (although the specific modality often awaited physiological testing, laser ablation, or mutant behavior). 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Some neurons change their principal wiring features during development, adding new synapses and deleting others (Walthall, 1990; White et al., 1978). Evidence is less solid regarding whether nematode neurons can modify their circuitry in response to the animal's experience, although their patterns of activity must surely vary according to this experience (Chao et al., 2004; Gomez et al., 2001; Peckol et al., 1999, 2001; Zhao and Nonet, 2000) (see Chapter 2). Regions important for sensory transduction in a nematode neuron are not always identifiable by their TEM structure alone, and thus certain cells evade easy categorization. For these reasons, the final tabulation of neuron subclasses has required occasional corrections as more physiological and developmental data has accumulated. The basic structure of a C. elegans neuron consists of a monopolar or bipolar cell extending one or two simple thin processes (neurites) along the length of the body (Fig. 1). The cell body is generally about 2 μm in diameter and contains a small compact nucleus. The neurites are extremely narrow in diameter (often just ≤0.2 μm) and most have virtually no local branches. Since the typical neuron is essentially unbranched, it must send its neurite along a local {"}neighborhood{"} in close proximity with its chosen partners before forming many synapses (White et al., 1983). Synapses occur en passant at local swellings along the length of a neurite (Fig. 2). A neurite often ends by making a gap junction (electrical synapse) where it contacts the neurite of a homologous neuron, such that neither cell extends a process into a territory occupied by its homologues (thus, the axon of VD4 will form junctions at its anterior and posterior limits with the axons of VD3 and VD5 in the ventral cord, and axons of left/right neuron pairs often form junctions where they meet in the nerve ring). 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N2 - The nematode nervous system is less centralized than those in higher animals (Bullock and Horridge, 1965), although the nerve ring in the head does bring together the majority of the body's neurons and synapses. The adult male also has enlarged tail ganglia (gaining 89 extra neurons) that function as a major processing center in the tail to control aspects of male mating behavior (discussed in Chapter 4). The largest proportion of synaptic neuropil is consolidated in the nerve ring itself. There is no separate neuropil associated with most clusters (ganglia) of cell bodies that surround the ring (Table I). Aside from the nerve ring and its extension beneath the nearby retrovesicular ganglion, the other principal sites of synaptic interactions consist of the ventral and dorsal nerve cords (discussed in Chapter 5) and in the preanal ganglion in the tail (Hall and Russell, 1991). A limited synaptic zone is associated with the egg-laying system at the vulva (Thomas et al., 1990). Synapses in other peripheral locales are rare. The nematode was the first eukaryote in which all neuronal and glial cell fates could be identified and characterized. The comprehensive nature of our knowledge of physical, molecular, and developmental aspects of these cells potentiates C. elegans as a model system for exploring both the development and function of complete behavioral circuits as well as the genetic specification of neuronal characters in isolation. Similarities between nematode neurons and those in other organisms include the early guidance receptors used for axon outgrowth, and the cellular machinery (e.g., vesicular transporters, ion channels, synaptic proteins) utilized to carry out mature functions (Ruvkun and Hobert, 1998) (see Chapter 3). The ligands used for cell signaling and the transmitters (both classical neurotransmitters [such as GABA, acetylcholine, serotonin, and so on] and neuropeptides) used in neuronal signaling are generally conserved as well (Bargmann, 1998) (see Chapter 3). Classification of nematode neurons into functional categories was initially done according to transmission electron microscopy (TEM) data alone (Albertson and Thomson, 1976; Hall, 1977; Sulston et al., 1980; Ward et al., 1975; Ware et al., 1975; White et al., 1976, 1986). Motor neurons comprised all of those cells that consistently formed neuromuscular junctions (NMJs) onto one or more muscle cells. Sensory neurons were those cells that possessed a distinct sensory dendrite of any modality (although the specific modality often awaited physiological testing, laser ablation, or mutant behavior). Interneurons comprised most of the rest; where their synaptic wiring imputed some role in collecting and relaying synaptic activity from upstream (sensory or interneuron) neurons to downstream effector neurons. Some neurons that have been categorized as "sensory" or "motor" cells may also have a high degree of interconnectivity that would also classify them as interneurons. Some neurons displayed dual roles ("polymodal"), for instance having both a sensory dendrite and NMJ outputs. Several neurons with few distinctive features were difficult to categorize. Anatomic and genetic studies have identified several "pioneer neurons" that play important roles in axon guidance or maintenance, while having little or no role in synaptic circuits (Aurelio et al., 2002; Chen et al., 2005; Durbin, 1987; Wadsworth et al., 1996). Some potential neurons undergo early apoptotic deaths soon after their birth and could not be categorized into a functional class (Sulston et al., 1983). Some neurons change their principal wiring features during development, adding new synapses and deleting others (Walthall, 1990; White et al., 1978). Evidence is less solid regarding whether nematode neurons can modify their circuitry in response to the animal's experience, although their patterns of activity must surely vary according to this experience (Chao et al., 2004; Gomez et al., 2001; Peckol et al., 1999, 2001; Zhao and Nonet, 2000) (see Chapter 2). Regions important for sensory transduction in a nematode neuron are not always identifiable by their TEM structure alone, and thus certain cells evade easy categorization. For these reasons, the final tabulation of neuron subclasses has required occasional corrections as more physiological and developmental data has accumulated. The basic structure of a C. elegans neuron consists of a monopolar or bipolar cell extending one or two simple thin processes (neurites) along the length of the body (Fig. 1). The cell body is generally about 2 μm in diameter and contains a small compact nucleus. The neurites are extremely narrow in diameter (often just ≤0.2 μm) and most have virtually no local branches. Since the typical neuron is essentially unbranched, it must send its neurite along a local "neighborhood" in close proximity with its chosen partners before forming many synapses (White et al., 1983). Synapses occur en passant at local swellings along the length of a neurite (Fig. 2). A neurite often ends by making a gap junction (electrical synapse) where it contacts the neurite of a homologous neuron, such that neither cell extends a process into a territory occupied by its homologues (thus, the axon of VD4 will form junctions at its anterior and posterior limits with the axons of VD3 and VD5 in the ventral cord, and axons of left/right neuron pairs often form junctions where they meet in the nerve ring). Thus, the nervous system is exceedingly economical not only in cell number but also in the number of processes or branches. Even the final positions of neuron cell bodies seem efficiently managed to minimize the total "wiring cost" of the nervous system (Chen et al., 2005). The total number of synapses per neuron is also remarkably limited. The hermaphrodite adult contains about 5000 chemical synapses, 700 gap junctions and 2000 NMJs. Many cells only form 25 to 50 synapses, and certain neurons form fewer than 10 synapses in total, including repeated contacts to the same partner. Even the most important command interneurons have about 200 synapses in total.

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Synapses in other peripheral locales are rare. The nematode was the first eukaryote in which all neuronal and glial cell fates could be identified and characterized. The comprehensive nature of our knowledge of physical, molecular, and developmental aspects of these cells potentiates C. elegans as a model system for exploring both the development and function of complete behavioral circuits as well as the genetic specification of neuronal characters in isolation. Similarities between nematode neurons and those in other organisms include the early guidance receptors used for axon outgrowth, and the cellular machinery (e.g., vesicular transporters, ion channels, synaptic proteins) utilized to carry out mature functions (Ruvkun and Hobert, 1998) (see Chapter 3). The ligands used for cell signaling and the transmitters (both classical neurotransmitters [such as GABA, acetylcholine, serotonin, and so on] and neuropeptides) used in neuronal signaling are generally conserved as well (Bargmann, 1998) (see Chapter 3). Classification of nematode neurons into functional categories was initially done according to transmission electron microscopy (TEM) data alone (Albertson and Thomson, 1976; Hall, 1977; Sulston et al., 1980; Ward et al., 1975; Ware et al., 1975; White et al., 1976, 1986). Motor neurons comprised all of those cells that consistently formed neuromuscular junctions (NMJs) onto one or more muscle cells. Sensory neurons were those cells that possessed a distinct sensory dendrite of any modality (although the specific modality often awaited physiological testing, laser ablation, or mutant behavior). Interneurons comprised most of the rest; where their synaptic wiring imputed some role in collecting and relaying synaptic activity from upstream (sensory or interneuron) neurons to downstream effector neurons. Some neurons that have been categorized as "sensory" or "motor" cells may also have a high degree of interconnectivity that would also classify them as interneurons. Some neurons displayed dual roles ("polymodal"), for instance having both a sensory dendrite and NMJ outputs. Several neurons with few distinctive features were difficult to categorize. Anatomic and genetic studies have identified several "pioneer neurons" that play important roles in axon guidance or maintenance, while having little or no role in synaptic circuits (Aurelio et al., 2002; Chen et al., 2005; Durbin, 1987; Wadsworth et al., 1996). Some potential neurons undergo early apoptotic deaths soon after their birth and could not be categorized into a functional class (Sulston et al., 1983). Some neurons change their principal wiring features during development, adding new synapses and deleting others (Walthall, 1990; White et al., 1978). Evidence is less solid regarding whether nematode neurons can modify their circuitry in response to the animal's experience, although their patterns of activity must surely vary according to this experience (Chao et al., 2004; Gomez et al., 2001; Peckol et al., 1999, 2001; Zhao and Nonet, 2000) (see Chapter 2). Regions important for sensory transduction in a nematode neuron are not always identifiable by their TEM structure alone, and thus certain cells evade easy categorization. For these reasons, the final tabulation of neuron subclasses has required occasional corrections as more physiological and developmental data has accumulated. The basic structure of a C. elegans neuron consists of a monopolar or bipolar cell extending one or two simple thin processes (neurites) along the length of the body (Fig. 1). The cell body is generally about 2 μm in diameter and contains a small compact nucleus. The neurites are extremely narrow in diameter (often just ≤0.2 μm) and most have virtually no local branches. Since the typical neuron is essentially unbranched, it must send its neurite along a local "neighborhood" in close proximity with its chosen partners before forming many synapses (White et al., 1983). Synapses occur en passant at local swellings along the length of a neurite (Fig. 2). A neurite often ends by making a gap junction (electrical synapse) where it contacts the neurite of a homologous neuron, such that neither cell extends a process into a territory occupied by its homologues (thus, the axon of VD4 will form junctions at its anterior and posterior limits with the axons of VD3 and VD5 in the ventral cord, and axons of left/right neuron pairs often form junctions where they meet in the nerve ring). Thus, the nervous system is exceedingly economical not only in cell number but also in the number of processes or branches. Even the final positions of neuron cell bodies seem efficiently managed to minimize the total "wiring cost" of the nervous system (Chen et al., 2005). The total number of synapses per neuron is also remarkably limited. The hermaphrodite adult contains about 5000 chemical synapses, 700 gap junctions and 2000 NMJs. Many cells only form 25 to 50 synapses, and certain neurons form fewer than 10 synapses in total, including repeated contacts to the same partner. Even the most important command interneurons have about 200 synapses in total.

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