Analyses of Habituation in Caenorhabditis elegans

Abstract

Although the nonassociative form of learning, habituation, is often described as the simplest form of learning, remarkably little is known about the cellular processes underlying its behavioral expression. Here, we review research on habituation in the nematode Caenorhabditis elegans that addresses habituation at behavioral, neural circuit, and genetic levels. This work highlights the need to understand the dynamics of a behavior before attempting to determine its underlying mechanism. In many cases knowing the characteristics of a behavior can direct or guide a search for underlying cellular mechanisms. We have highlighted the importance of interstimulus interval (ISI) in both short-and long-term habituation and suggested that different cellular mechanisms might underlie habituation at different ISIs. Like other organisms, C. elegans shows both accumulation of habituation with repeated training blocks and long-term retention of spaced or distributed training, but not for massed training. Exposure to heat shock during the interblock intervals eliminates the long-term memory for habituation but not the accumulation of short-term habituation over blocks of training. Analyses using laser ablation of identified neurons, and of identified mutants have shown that there are multiple sites of plasticity for the response and that glutamate plays a role in long-term retention of habituation training.

Touch sensitivity in Caenorhabditis elegans

“…These results suggest that the mechanisms of habituation for tap withdrawal response differ for short and long ISIs [61,65]. Training C. elegans with blocks of taps at longer ISIs produces long-term memory (LTM) for habituation that can be retained in optimal conditions for about 24 h. This memory cannot be generated with training blocks of short ISIs and can be disrupted by heat-shocking the animals in between blocks of stimuli [6,65]. C. elegans are also susceptible to context conditioning, as plate tap training at long ISIs can be associated with other environmental cues to increase retention of habituation [58].…”

“…This phenomenon is known as habituation. Habituation to gentle touch has been studied primarily by Catharine Rankin and her colleagues using the tap-withdrawal response [65]. Plate tap causes mature animals to reverse, and the frequency and distance of reversals diminish progressively with repeated taps.…”

“…Worms trained at shorter ISIs spontaneously recover from habituation quicker than worms trained at longer ISIs. These results suggest that the mechanisms of habituation for tap withdrawal response differ for short and long ISIs [61,65]. Training C. elegans with blocks of taps at longer ISIs produces long-term memory (LTM) for habituation that can be retained in optimal conditions for about 24 h. This memory cannot be generated with training blocks of short ISIs and can be disrupted by heat-shocking the animals in between blocks of stimuli [6,65].…”

Conservation of gene function in behaviour

“…Another is sensitization, an increase in response to a neutral stimulus following exposure to a stronger stimulus. Habituation and sensitization are observed in species as diverse as C. elegans [55], D. melanogaster [56], Rattus norvegicus [57] and humans [58]. Associative learning has also been observed in many species [59,60].…”

Protection from premature habituation requires functional mushroom bodies in Drosophila

“…Habituation is a major mechanism to decrease responsiveness to repetitive or prolonged nonreinforced stimuli (Thomson and Spencer 1966;Groves and Thomson 1970;Rankin 2000;Rose and Rankin 2001). Because response attenuation depends on prior experience of a stimulus, habituation has been studied as a form of nonassociative learning in a variety of models (Hawkins 1988;Burrell and Sahley 1998;Rose and Rankin 2001;Deshmukh and Bhalla 2003;Ezzeddine and Glanzman 2003).…”