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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

There were changes in habituation of response probability throughout middle-age in wild-type worms. This graph shows response probability habituation for 72-, 84-, 96-, 108-, and 120-h-old (all reproductive adults) wild-type C. elegans in response to a series of 30 taps. Age was significantly related to the probability of responding to the final tap at both a 10-s ISI (A) and at a 60-s ISI (B) (Timbers et al., 2013).
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Figure 6: There were changes in habituation of response probability throughout middle-age in wild-type worms. This graph shows response probability habituation for 72-, 84-, 96-, 108-, and 120-h-old (all reproductive adults) wild-type C. elegans in response to a series of 30 taps. Age was significantly related to the probability of responding to the final tap at both a 10-s ISI (A) and at a 60-s ISI (B) (Timbers et al., 2013).

Mentions: In addition to experience dependent changes during development, the ability to learn and remember also alters with normal aging. Beck and Rankin (1993) studied aging C. elegans (10 and 12 days post-hatching) and found that they habituated more rapidly and showed less spontaneous recovery than middle-aged adults. This is not unexpected as C. elegans rapidly begins to show nervous system and muscle breakdown after it has passed its reproductive prime (Pan et al., 2011). However, what about during middle age, before the neurons and muscles show evidence of degeneration? Are there changes in sensory plasticity during this period? Worms develop from fertilized egg to reproductive young adult in 3.5 days; they then are reproductive adults for 3–4 days, before becoming senescent (Wood et al., 1980). Timbers et al. (2013) investigated whether there were age-dependent changes in habituation in middle-aged C. elegans. They tested the effect of age on tap habituation in populations of worms 72 (day 0 of adulthood), 84, 96, 108, and 120 (day 2.5 of adulthood) h old. They found that habituation of reversal probability to tap in young animals (72 h old) occurred more slowly than for older adult (120 h) animals (Figure 6). The factors responsible for this difference between 72 and 120 h old worms might be in the transduction of the tap stimulus or might reflect some change in cell excitability or synaptic strength as worms aged. To investigate this Timbers et al. used transgenic worms expressing Channelrhodopsin-2 (blue light-gated cation channel) in the touch cells (Nagel et al., 2003; Boyden et al., 2005). Applying a short pulse of blue light to the transgenic worms activates the touch cells and induces a reversal response similar to that seen following a mechanical tap. If activation of the touch cells by blue light showed the same results as applying taps in adult worms (72, 84, 96, and 120 h old), the age-dependent changes in behavior must originate downstream of sensory transduction. However, the results of this experiment showed that age was not related to the probability of responding to repeated blue light pulses, suggesting that the age-dependent changes in behavior originate upstream of cellular depolarization. A known characteristic of habituation is that less intense stimuli cause more habituation, whereas more intense stimuli cause less habituation (Thompson and Spencer, 1966; Groves and Thompson, 1970; Rankin et al., 2009). Consistent with this body of literature, Timbers et al. (2013) also showed an association between stimulus intensity and habituation of young adult worms (72 h-old), however, older worms showed no such association. Thus, the rate of reversal probability habituation is dependent on the ability to discriminate stimulus intensity, which the younger worms seem to do to a greater extent than the older worms. Possible explanations for the decrement in stimulus discrimination with age include changes in neuronal excitability, changes in the thickness of the cuticle or in the strength of the connection of the mechanosensory cells to the body wall (Timbers et al., 2013).


Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit.

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

There were changes in habituation of response probability throughout middle-age in wild-type worms. This graph shows response probability habituation for 72-, 84-, 96-, 108-, and 120-h-old (all reproductive adults) wild-type C. elegans in response to a series of 30 taps. Age was significantly related to the probability of responding to the final tap at both a 10-s ISI (A) and at a 60-s ISI (B) (Timbers et al., 2013).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: There were changes in habituation of response probability throughout middle-age in wild-type worms. This graph shows response probability habituation for 72-, 84-, 96-, 108-, and 120-h-old (all reproductive adults) wild-type C. elegans in response to a series of 30 taps. Age was significantly related to the probability of responding to the final tap at both a 10-s ISI (A) and at a 60-s ISI (B) (Timbers et al., 2013).
Mentions: In addition to experience dependent changes during development, the ability to learn and remember also alters with normal aging. Beck and Rankin (1993) studied aging C. elegans (10 and 12 days post-hatching) and found that they habituated more rapidly and showed less spontaneous recovery than middle-aged adults. This is not unexpected as C. elegans rapidly begins to show nervous system and muscle breakdown after it has passed its reproductive prime (Pan et al., 2011). However, what about during middle age, before the neurons and muscles show evidence of degeneration? Are there changes in sensory plasticity during this period? Worms develop from fertilized egg to reproductive young adult in 3.5 days; they then are reproductive adults for 3–4 days, before becoming senescent (Wood et al., 1980). Timbers et al. (2013) investigated whether there were age-dependent changes in habituation in middle-aged C. elegans. They tested the effect of age on tap habituation in populations of worms 72 (day 0 of adulthood), 84, 96, 108, and 120 (day 2.5 of adulthood) h old. They found that habituation of reversal probability to tap in young animals (72 h old) occurred more slowly than for older adult (120 h) animals (Figure 6). The factors responsible for this difference between 72 and 120 h old worms might be in the transduction of the tap stimulus or might reflect some change in cell excitability or synaptic strength as worms aged. To investigate this Timbers et al. used transgenic worms expressing Channelrhodopsin-2 (blue light-gated cation channel) in the touch cells (Nagel et al., 2003; Boyden et al., 2005). Applying a short pulse of blue light to the transgenic worms activates the touch cells and induces a reversal response similar to that seen following a mechanical tap. If activation of the touch cells by blue light showed the same results as applying taps in adult worms (72, 84, 96, and 120 h old), the age-dependent changes in behavior must originate downstream of sensory transduction. However, the results of this experiment showed that age was not related to the probability of responding to repeated blue light pulses, suggesting that the age-dependent changes in behavior originate upstream of cellular depolarization. A known characteristic of habituation is that less intense stimuli cause more habituation, whereas more intense stimuli cause less habituation (Thompson and Spencer, 1966; Groves and Thompson, 1970; Rankin et al., 2009). Consistent with this body of literature, Timbers et al. (2013) also showed an association between stimulus intensity and habituation of young adult worms (72 h-old), however, older worms showed no such association. Thus, the rate of reversal probability habituation is dependent on the ability to discriminate stimulus intensity, which the younger worms seem to do to a greater extent than the older worms. Possible explanations for the decrement in stimulus discrimination with age include changes in neuronal excitability, changes in the thickness of the cuticle or in the strength of the connection of the mechanosensory cells to the body wall (Timbers et al., 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