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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

Genes tested for their role in long- and short-term memory for non-associative habituation and associative context conditioning. Three genes were tested, crh-1 which is the worm homologue of CREB, glr-1 the worm homologue of a glutamate AMPA-type receptor subunit and nmr-1 the worm homologue of an NMDA-type glutamate receptor subunit. The results indicated that nmr-1 is required for short and long-term context conditioning but not necessary for non-associative learning; crh-1 is critical for long-term but not short-term memory for both associative and non-associative memory and that glr-1 is not required for short-term non-associative learning, but required for long term as well as short- and long-term context conditioning [Based on data from Lau et al. (2013)].
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Figure 5: Genes tested for their role in long- and short-term memory for non-associative habituation and associative context conditioning. Three genes were tested, crh-1 which is the worm homologue of CREB, glr-1 the worm homologue of a glutamate AMPA-type receptor subunit and nmr-1 the worm homologue of an NMDA-type glutamate receptor subunit. The results indicated that nmr-1 is required for short and long-term context conditioning but not necessary for non-associative learning; crh-1 is critical for long-term but not short-term memory for both associative and non-associative memory and that glr-1 is not required for short-term non-associative learning, but required for long term as well as short- and long-term context conditioning [Based on data from Lau et al. (2013)].

Mentions: The genetic analyses of short and long-term habituation and context dependent habituation showed that each of the genes tested had a different pattern of results (Figure 5). CREB has been shown to be critical for LTM in various species (e.g., Bernabeu et al., 1997; Josselyn et al., 2004) and worms with a mutation in crh-1 (homolog of CREB in C. elegans) show normal short-term habituation but no LTM (Timbers and Rankin, 2011). For context conditioning experiments, Lau et al. found that worms with a mutation in crh-1 showed short-term habituation and short-term context conditioning but no long-term context conditioning. Rescuing CRH-1 in mutant worms rescued the long-term context conditioning deficit. In previous studies, it was shown that glr-1 (encoding a non-NMDA-type glutamate receptor subunit) is critical for LTM performance, but not necessary for short-term memory (Rose et al., 2002). Lau et al. found that in addition to not showing long-term habituation, glr-1 mutants did not show short-term or long-term context conditioning. nmr-1 encodes an NMDA-type glutamate receptor subunit broadly expressed in interneurons of the mechanosensory circuit in C. elegans. Lau et al. (2013) showed that an nmr-1 mutant did not show any deficit in short-term or LTM for habituation, however, NMR-1 was critical for both short- and long-term context effects in habituation. How is the input from the two sensory systems integrated? Previous studies showed that expression of nmr-1 in the pair of RIM interneurons was essential for starvation and taste association learning (Kano et al., 2008). Based on this, Lau et al. (2013) investigated the role of nmr-1 in RIM interneurons by cell-specific rescue of this gene and found that expression of NMR-1 in the RIM interneurons was sufficient to rescue both short- and long-term context conditioning in nmr-1 mutant animals. This suggested that the interneuron RIM is a key site of integration for sensory input from chemosensory and mechanosensory neurons. Context conditioning learning in the mechanosensory circuit of C. elegans offers a new opportunity to investigate the genes critical for short- and long-term associative and non-associative learning as well as to study how sensory integration is encoded in the memories.


Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit.

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

Genes tested for their role in long- and short-term memory for non-associative habituation and associative context conditioning. Three genes were tested, crh-1 which is the worm homologue of CREB, glr-1 the worm homologue of a glutamate AMPA-type receptor subunit and nmr-1 the worm homologue of an NMDA-type glutamate receptor subunit. The results indicated that nmr-1 is required for short and long-term context conditioning but not necessary for non-associative learning; crh-1 is critical for long-term but not short-term memory for both associative and non-associative memory and that glr-1 is not required for short-term non-associative learning, but required for long term as well as short- and long-term context conditioning [Based on data from Lau et al. (2013)].
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Genes tested for their role in long- and short-term memory for non-associative habituation and associative context conditioning. Three genes were tested, crh-1 which is the worm homologue of CREB, glr-1 the worm homologue of a glutamate AMPA-type receptor subunit and nmr-1 the worm homologue of an NMDA-type glutamate receptor subunit. The results indicated that nmr-1 is required for short and long-term context conditioning but not necessary for non-associative learning; crh-1 is critical for long-term but not short-term memory for both associative and non-associative memory and that glr-1 is not required for short-term non-associative learning, but required for long term as well as short- and long-term context conditioning [Based on data from Lau et al. (2013)].
Mentions: The genetic analyses of short and long-term habituation and context dependent habituation showed that each of the genes tested had a different pattern of results (Figure 5). CREB has been shown to be critical for LTM in various species (e.g., Bernabeu et al., 1997; Josselyn et al., 2004) and worms with a mutation in crh-1 (homolog of CREB in C. elegans) show normal short-term habituation but no LTM (Timbers and Rankin, 2011). For context conditioning experiments, Lau et al. found that worms with a mutation in crh-1 showed short-term habituation and short-term context conditioning but no long-term context conditioning. Rescuing CRH-1 in mutant worms rescued the long-term context conditioning deficit. In previous studies, it was shown that glr-1 (encoding a non-NMDA-type glutamate receptor subunit) is critical for LTM performance, but not necessary for short-term memory (Rose et al., 2002). Lau et al. found that in addition to not showing long-term habituation, glr-1 mutants did not show short-term or long-term context conditioning. nmr-1 encodes an NMDA-type glutamate receptor subunit broadly expressed in interneurons of the mechanosensory circuit in C. elegans. Lau et al. (2013) showed that an nmr-1 mutant did not show any deficit in short-term or LTM for habituation, however, NMR-1 was critical for both short- and long-term context effects in habituation. How is the input from the two sensory systems integrated? Previous studies showed that expression of nmr-1 in the pair of RIM interneurons was essential for starvation and taste association learning (Kano et al., 2008). Based on this, Lau et al. (2013) investigated the role of nmr-1 in RIM interneurons by cell-specific rescue of this gene and found that expression of NMR-1 in the RIM interneurons was sufficient to rescue both short- and long-term context conditioning in nmr-1 mutant animals. This suggested that the interneuron RIM is a key site of integration for sensory input from chemosensory and mechanosensory neurons. Context conditioning learning in the mechanosensory circuit of C. elegans offers a new opportunity to investigate the genes critical for short- and long-term associative and non-associative learning as well as to study how sensory integration is encoded in the memories.

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