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Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit.

Bozorgmehr T, Ardiel EL, McEwan AH, Rankin CH - Front Physiol (2013)

Bottom Line: As worms develop through young adult and adult stages there is a shift toward deeper habituation of response probability that is likely the result of changes in sensitivity to stimulus intensity.Overall, the mechanosensory system of C. elegans shows a great deal of experience dependent plasticity both during development and as an adult.The simplest form of learning, habituation, is not so simple and is mediated and/or modulated by a number of different processes, some of which we are beginning to understand.

View Article: PubMed Central - PubMed

Affiliation: Brain Research Centre, University of British Columbia Vancouver, BC, Canada.

ABSTRACT
Despite having a small nervous system (302 neurons) and relatively short lifespan (14-21 days), the nematode Caenorhabditis elegans has a substantial ability to change its behavior in response to experience. The behavior discussed here is the tap withdrawal response, whereby the worm crawls backwards a brief distance in response to a non-localized mechanosensory stimulus from a tap to the side of the Petri plate within which it lives. The neural circuit that underlies this behavior is primarily made up of five sensory neurons and four pairs of interneurons. In this review we describe two classes of mechanosensory plasticity: adult learning and memory and experience dependent changes during development. As worms develop through young adult and adult stages there is a shift toward deeper habituation of response probability that is likely the result of changes in sensitivity to stimulus intensity. Adult worms show short- intermediate- and long-term habituation as well as context dependent habituation. Short-term habituation requires glutamate signaling and auto-phosphorylation of voltage-dependent potassium channels and is modulated by dopamine signaling in the mechanosensory neurons. Long-term memory (LTM) for habituation is mediated by down-regulation of expression of an AMPA-type glutamate receptor subunit. Intermediate memory involves an increase in release of an inhibitory neuropeptide. Depriving larval worms of mechanosensory stimulation early in development leads to fewer synaptic vesicles in the mechanosensory neurons and lower levels of an AMPA-type glutamate receptor subunit in the interneurons. Overall, the mechanosensory system of C. elegans shows a great deal of experience dependent plasticity both during development and as an adult. The simplest form of learning, habituation, is not so simple and is mediated and/or modulated by a number of different processes, some of which we are beginning to understand.

No MeSH data available.


Related in: MedlinePlus

The circuit mediating the response to tap. The touch cells are represented by ovals (blue), the interneurons by stars (yellow), and the motor neurons by rectangles (red). All neurons are bilaterally symmetrical, except AVM and DVA. The neurons in green, PVD and DVA, contribute to both forward and backward movement and may play a role in integrating the two responses. Arrows and dashed lines denote chemical and electrical connections, respectively, thickness of lines reflects relative number of synapses [Based on data from Chalfie et al. (1985), Wicks and Rankin (1995)].
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Figure 1: The circuit mediating the response to tap. The touch cells are represented by ovals (blue), the interneurons by stars (yellow), and the motor neurons by rectangles (red). All neurons are bilaterally symmetrical, except AVM and DVA. The neurons in green, PVD and DVA, contribute to both forward and backward movement and may play a role in integrating the two responses. Arrows and dashed lines denote chemical and electrical connections, respectively, thickness of lines reflects relative number of synapses [Based on data from Chalfie et al. (1985), Wicks and Rankin (1995)].

Mentions: C. elegans has a variety of sensory neurons that respond to mechanical stimuli. Activity of the touch neurons, proprioceptors, and nociceptors are modulated by mechanical force. Two protein superfamilies' are essential for transforming mechanical stimuli into electrical signals by changing the ionic current in mechanosensory neurons: the TRP channels, and the DEG/ENaC channels. TRP channels are non-specific cation channels composed of six transmembrane alpha helix subunits, while DEG/ENaC channels are predominantly permeable to sodium and in some cases to calcium and consist of two transmembrane alpha helices. The mechanism of mechanotransduction has been broadly studied in C. elegans and over 10% of the neurons in the adult hermaphrodite are sensitive to external touch stimuli (Chatzigeorgiou and Schafer, 2011). The best studied of the mechanosensory circuits are the head and tail touch circuits: when a worm is touched lightly on the head it crawls backwards away from the stimulus; when a worm is touched lightly on the tail it crawls forwards away from the stimulus. The touch cell anatomical wiring diagram was determined by serial section electron micrographs (Sulston et al., 1980; White et al., 1986). Subsequently, Chalfie et al. (1985) used laser ablation of neurons to determine the function of cells in the head and tail touch circuits. By killing cells and assaying touch responses Chalfie et al. showed that response to gentle touch to the body was mediated by three mechanosensory neurons in the head (ALML, ALMR, and AVM) and by two mechanosensory neurons in the tail PLML and PLMR. In addition four pairs of interneurons were implicated: AVD, PVC, AVA, and AVB, which are often called command interneurons and integrate information onto motor neurons. Laser ablation showed that AVD and AVA are required for moving backwards to anterior touch, while PVC and AVB are involved in moving forward to posterior touch. The five touch-receptor neurons [ALM (L/R), PLM (L/R), AVM] have a very simple structure. Each cell has a single long process that ends in a synaptic branch. These neurons make synapses at synaptic branches, and along their processes (Chalfie et al., 1985). At the time of hatching ALML and ALMR are located on the left and right side, respectively, in the anterior half of the worm while PLML and PLMR are on the left and right in the posterior. AVM develops post-embryonically and is located in a ventral position (Chalfie and Sulston, 1981). In addition to light touch, the same five mechanosensory neurons respond to a mechanical stimulus delivered to the side of the agar-filled petri plate holding the worm. This vibrational stimulus is called a tap (Rankin et al., 1990) and is thought to simultaneously activate the head and tail touch circuits. In response to tap worms crawl backwards for a short distance. Through laser ablation Wicks and Rankin (1995) confirmed that the five sensory neurons and four pairs of interneurons described in Chalfie et al. (1985) were also critical for the tap withdrawal response. Wicks and Rankin (1995) also hypothesized that DVA and PVD neurons play a role in integrating the sensory input coming from the head and tail (Figure 1). The head and tail input triggers movement in opposite directions; the direction of movement in response to tap is thought to be dependent on imbalanced activity between forward (two sensory neurons) and backward (three neurons) sub-circuits (Chalfie et al., 1985; Wicks and Rankin, 1995). Chiba and Rankin (1990) showed that, before the post-embryonic AVM neuron develops, the circuit is balanced with two sensory neurons for each head and tail, and the behavior consists of 50% forward and 50% backward locomotion in response to tap. When AVM connects to the circuit the bias shifts to reversals (>85% of responses).


Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit.

Bozorgmehr T, Ardiel EL, McEwan AH, Rankin CH - Front Physiol (2013)

The circuit mediating the response to tap. The touch cells are represented by ovals (blue), the interneurons by stars (yellow), and the motor neurons by rectangles (red). All neurons are bilaterally symmetrical, except AVM and DVA. The neurons in green, PVD and DVA, contribute to both forward and backward movement and may play a role in integrating the two responses. Arrows and dashed lines denote chemical and electrical connections, respectively, thickness of lines reflects relative number of synapses [Based on data from Chalfie et al. (1985), Wicks and Rankin (1995)].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750945&req=5

Figure 1: The circuit mediating the response to tap. The touch cells are represented by ovals (blue), the interneurons by stars (yellow), and the motor neurons by rectangles (red). All neurons are bilaterally symmetrical, except AVM and DVA. The neurons in green, PVD and DVA, contribute to both forward and backward movement and may play a role in integrating the two responses. Arrows and dashed lines denote chemical and electrical connections, respectively, thickness of lines reflects relative number of synapses [Based on data from Chalfie et al. (1985), Wicks and Rankin (1995)].
Mentions: C. elegans has a variety of sensory neurons that respond to mechanical stimuli. Activity of the touch neurons, proprioceptors, and nociceptors are modulated by mechanical force. Two protein superfamilies' are essential for transforming mechanical stimuli into electrical signals by changing the ionic current in mechanosensory neurons: the TRP channels, and the DEG/ENaC channels. TRP channels are non-specific cation channels composed of six transmembrane alpha helix subunits, while DEG/ENaC channels are predominantly permeable to sodium and in some cases to calcium and consist of two transmembrane alpha helices. The mechanism of mechanotransduction has been broadly studied in C. elegans and over 10% of the neurons in the adult hermaphrodite are sensitive to external touch stimuli (Chatzigeorgiou and Schafer, 2011). The best studied of the mechanosensory circuits are the head and tail touch circuits: when a worm is touched lightly on the head it crawls backwards away from the stimulus; when a worm is touched lightly on the tail it crawls forwards away from the stimulus. The touch cell anatomical wiring diagram was determined by serial section electron micrographs (Sulston et al., 1980; White et al., 1986). Subsequently, Chalfie et al. (1985) used laser ablation of neurons to determine the function of cells in the head and tail touch circuits. By killing cells and assaying touch responses Chalfie et al. showed that response to gentle touch to the body was mediated by three mechanosensory neurons in the head (ALML, ALMR, and AVM) and by two mechanosensory neurons in the tail PLML and PLMR. In addition four pairs of interneurons were implicated: AVD, PVC, AVA, and AVB, which are often called command interneurons and integrate information onto motor neurons. Laser ablation showed that AVD and AVA are required for moving backwards to anterior touch, while PVC and AVB are involved in moving forward to posterior touch. The five touch-receptor neurons [ALM (L/R), PLM (L/R), AVM] have a very simple structure. Each cell has a single long process that ends in a synaptic branch. These neurons make synapses at synaptic branches, and along their processes (Chalfie et al., 1985). At the time of hatching ALML and ALMR are located on the left and right side, respectively, in the anterior half of the worm while PLML and PLMR are on the left and right in the posterior. AVM develops post-embryonically and is located in a ventral position (Chalfie and Sulston, 1981). In addition to light touch, the same five mechanosensory neurons respond to a mechanical stimulus delivered to the side of the agar-filled petri plate holding the worm. This vibrational stimulus is called a tap (Rankin et al., 1990) and is thought to simultaneously activate the head and tail touch circuits. In response to tap worms crawl backwards for a short distance. Through laser ablation Wicks and Rankin (1995) confirmed that the five sensory neurons and four pairs of interneurons described in Chalfie et al. (1985) were also critical for the tap withdrawal response. Wicks and Rankin (1995) also hypothesized that DVA and PVD neurons play a role in integrating the sensory input coming from the head and tail (Figure 1). The head and tail input triggers movement in opposite directions; the direction of movement in response to tap is thought to be dependent on imbalanced activity between forward (two sensory neurons) and backward (three neurons) sub-circuits (Chalfie et al., 1985; Wicks and Rankin, 1995). Chiba and Rankin (1990) showed that, before the post-embryonic AVM neuron develops, the circuit is balanced with two sensory neurons for each head and tail, and the behavior consists of 50% forward and 50% backward locomotion in response to tap. When AVM connects to the circuit the bias shifts to reversals (>85% of responses).

Bottom Line: As worms develop through young adult and adult stages there is a shift toward deeper habituation of response probability that is likely the result of changes in sensitivity to stimulus intensity.Overall, the mechanosensory system of C. elegans shows a great deal of experience dependent plasticity both during development and as an adult.The simplest form of learning, habituation, is not so simple and is mediated and/or modulated by a number of different processes, some of which we are beginning to understand.

View Article: PubMed Central - PubMed

Affiliation: Brain Research Centre, University of British Columbia Vancouver, BC, Canada.

ABSTRACT
Despite having a small nervous system (302 neurons) and relatively short lifespan (14-21 days), the nematode Caenorhabditis elegans has a substantial ability to change its behavior in response to experience. The behavior discussed here is the tap withdrawal response, whereby the worm crawls backwards a brief distance in response to a non-localized mechanosensory stimulus from a tap to the side of the Petri plate within which it lives. The neural circuit that underlies this behavior is primarily made up of five sensory neurons and four pairs of interneurons. In this review we describe two classes of mechanosensory plasticity: adult learning and memory and experience dependent changes during development. As worms develop through young adult and adult stages there is a shift toward deeper habituation of response probability that is likely the result of changes in sensitivity to stimulus intensity. Adult worms show short- intermediate- and long-term habituation as well as context dependent habituation. Short-term habituation requires glutamate signaling and auto-phosphorylation of voltage-dependent potassium channels and is modulated by dopamine signaling in the mechanosensory neurons. Long-term memory (LTM) for habituation is mediated by down-regulation of expression of an AMPA-type glutamate receptor subunit. Intermediate memory involves an increase in release of an inhibitory neuropeptide. Depriving larval worms of mechanosensory stimulation early in development leads to fewer synaptic vesicles in the mechanosensory neurons and lower levels of an AMPA-type glutamate receptor subunit in the interneurons. Overall, the mechanosensory system of C. elegans shows a great deal of experience dependent plasticity both during development and as an adult. The simplest form of learning, habituation, is not so simple and is mediated and/or modulated by a number of different processes, some of which we are beginning to understand.

No MeSH data available.


Related in: MedlinePlus