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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

(A) Representative images of GLR-1::GFP expression in interneurons of the posterior ventral nerve cord in a worm that had been given spaced training for long-term memory for habituation 24 h before and an untrained control worm. There were significantly smaller GFP clusters in the trained worms than in the control worms. (B) Representative images of the vesicles in tap sensory neuron terminals visualized with a synaptobrevin GFP marker in control and trained worms. There was no difference in measured GFP expression between the trained and control worms (Rose et al., 2003).
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Figure 4: (A) Representative images of GLR-1::GFP expression in interneurons of the posterior ventral nerve cord in a worm that had been given spaced training for long-term memory for habituation 24 h before and an untrained control worm. There were significantly smaller GFP clusters in the trained worms than in the control worms. (B) Representative images of the vesicles in tap sensory neuron terminals visualized with a synaptobrevin GFP marker in control and trained worms. There was no difference in measured GFP expression between the trained and control worms (Rose et al., 2003).

Mentions: In Aplysia long-term habituation is mediated by a down regulation of vesicles in the siphon sensory neurons (Bailey and Chen, 1991). In mammals LTD (a lasting decrease in synaptic strength similar to long-term habituation) is mediated by down-regulation of AMPA-type glutamate receptors on the post-synaptic neurons. To determine whether LTM training for habituation was associated with changes in the sensory neurons or the command interneurons, worms carrying transgenes with green fluorescent protein fused to pre- and post-synaptic markers were given long-term habituation training and then imaged. One strain expressed GFP marking a synaptic vesicle protein, synaptobrevin (snb-1), in the mechanosensory neurons (Nonet, 1999). The other expressed GFP tagged GLR-1 receptor subunits (Rongo and Kaplan, 1999). The results showed no presynaptic changes in GFP tagged snb-1, however, spaced training for LTM induced a reduction in the size, but not the number, of GLR-1::GFP puncta in the posterior ventral nerve cord (Figure 4) Rose et al. (2003). Based on these results Rose et al hypothesized that the size of synapses was reduced by memory training, however, the number of synapses was not changed. Interestingly, with more training blocks over several days, decreases were seen in synaptbrevin GFP in the sensory neurons suggesting that plasticity in the sensory neurons requires more stimulation than plasticity of glutamate receptor trafficking in the command interneurons.


Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit.

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

(A) Representative images of GLR-1::GFP expression in interneurons of the posterior ventral nerve cord in a worm that had been given spaced training for long-term memory for habituation 24 h before and an untrained control worm. There were significantly smaller GFP clusters in the trained worms than in the control worms. (B) Representative images of the vesicles in tap sensory neuron terminals visualized with a synaptobrevin GFP marker in control and trained worms. There was no difference in measured GFP expression between the trained and control worms (Rose et al., 2003).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: (A) Representative images of GLR-1::GFP expression in interneurons of the posterior ventral nerve cord in a worm that had been given spaced training for long-term memory for habituation 24 h before and an untrained control worm. There were significantly smaller GFP clusters in the trained worms than in the control worms. (B) Representative images of the vesicles in tap sensory neuron terminals visualized with a synaptobrevin GFP marker in control and trained worms. There was no difference in measured GFP expression between the trained and control worms (Rose et al., 2003).
Mentions: In Aplysia long-term habituation is mediated by a down regulation of vesicles in the siphon sensory neurons (Bailey and Chen, 1991). In mammals LTD (a lasting decrease in synaptic strength similar to long-term habituation) is mediated by down-regulation of AMPA-type glutamate receptors on the post-synaptic neurons. To determine whether LTM training for habituation was associated with changes in the sensory neurons or the command interneurons, worms carrying transgenes with green fluorescent protein fused to pre- and post-synaptic markers were given long-term habituation training and then imaged. One strain expressed GFP marking a synaptic vesicle protein, synaptobrevin (snb-1), in the mechanosensory neurons (Nonet, 1999). The other expressed GFP tagged GLR-1 receptor subunits (Rongo and Kaplan, 1999). The results showed no presynaptic changes in GFP tagged snb-1, however, spaced training for LTM induced a reduction in the size, but not the number, of GLR-1::GFP puncta in the posterior ventral nerve cord (Figure 4) Rose et al. (2003). Based on these results Rose et al hypothesized that the size of synapses was reduced by memory training, however, the number of synapses was not changed. Interestingly, with more training blocks over several days, decreases were seen in synaptbrevin GFP in the sensory neurons suggesting that plasticity in the sensory neurons requires more stimulation than plasticity of glutamate receptor trafficking in the command interneurons.

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