Short-Term and Long-Term Habituation
Two types of habituation can be distinguished on the basis of the speed of recovery of the habituated response after training. In short-term habituation, the response recovers almost completely within hours. In long-term habitnation, the response can remain suppressed for days after training. Different mechanisms are at work in each case.
The amount and distribution of training trials determine whether short-term or longterm habituation would be observed. Activity induced by a shadow in the crab C. granulatus habituated significantly during the session after 5 or 10 training trials, but the response was fully recovered a day later (short-term habituation). However, increasing the amount of training to 15 trials or more led to substantial response decrement a day later (long-term habituation) (Pedreira, Romano, Tomsic, Lozada, & Maldonado, 1998). The distribution of trials in time also determines recovery speed. In A. californica, 40 training trials administered in a single session led to complete recovery a day after training (short-term habituation). However, habituation induced by 40 trials distributed over four daily sessions of 10 trials was still observable a week after training (long-term habituation) (Carew, Pinsker, & Kandel, 1972).
Neural Basis of Short-Term Habituation
Several features make habituation a good candidate model for the cellular analysis of a simple form of learning. The behavioral properties of habituation are well established and the neural circuit of some of the reflexes that exhibit habituation is also known. Habituation can help us understand one of the most intriguing aspects of neural functioning: How is information acquired and stored in the CNS?
The following sections capitalize on the extensive analyses of habituation in two model systems: the nematode Caenorhabditis elegans and the mollusk Aplysia californica.
The Nematode Caenorhabditis elegans
The nematode C. elegans is an attractive model system for several reasons: It has only 302 neurons (a fixed number for the species), the location of individual neurons and their synaptic connections varies little across animals, and the approximately 5,000 chemical synapses and 2,000 electrical synapses have been mapped (White, Southgate, Thompson, & Brenner, 1986). One preparation involves the tap-withdrawal response (TWR). Tapping the plate where the animal is placed produces a vibration of the substrate that induces reverse swimming. Reverse swimming also occurs spontaneously and can be induced by thermal stimuli (a heated plate placed close to the nematode, but without touching the animal or the medium through which the animal is moving).
Short-term habituation of the TWR shows many properties of habituation, including dishabituation (Rankin, Beck, & Chiba, 1990). Dishabituation is observed when the habituated TWR recovers after a mild shock to the head of the animal, suggesting that the mechanisms of habituation involve synaptic changes. Although reverse swimming responses that occur in response to tapping are mediated by the same locomotor CPG underlying spontaneous reverse swimming, when the TWR is habituated, the number and frequency of spontaneous reverse swimming responses is not affected (McEwan & Rankin, 2013). Similarly, reverse swimming elicited by a thermal stimulus is not affected by prior habituation of that response by tapping. This suggests that habituation of the TWR occurs within the pathway involving mechanoreceptors, rather than in the locomotor pattern generators or motoneurons controlling reverse swimming. If the latter were true, then habituation of the TWR should have affected both spontaneous reverse swimming and the reverse swimming elicited by stimuli other than tapping.
The Mollusk Aplysia californica
The site responsible for short-term habituation has been identified in the gill-withdrawal reflex (GWR) of the mollusk Aplysia. The GWR has a monosynaptic pathway connecting sensory neurons carrying information from the siphon and motoneurons innervating the gill
Simple Nervous Systems and Behavior 117 muscles (see Figure 4.4). The critical synapse is located in the abdominal ganglion. This ganglion can be isolated and maintained in a seawater solution long enough to perform habituation experiments (Castellucci & Kandel, 1974). The nerve carrying sensory information from the siphon can be electrically stimulated (the habituating stimulus), and activity of one of the critical motoneurons, L7, can be monitored as an output (the response). Repeated activation of the sensory neuron does not affect its own ability to generate an AP, but the EPSP elicited on L7 decreases in magnitude. EPSP changes are not caused by interneurons, but result from the repeated activation of the sensory-motor synapse. Interestingly, if L7 is repeatedly stimulated, its ability to produce an AP is not diminished, suggesting that the source of synaptic plasticity is in the presynaptic sensory neuron or in the sensory-motor synapse.
Because short-term habituation of the GWR is mediated by a single synapse that undergoes a decrease in its elicited amplitude, the phenomenon is known as homosynaptic depression. Homosynaptic depression is caused by a decrease in the amount of glutamate neurotransmitter released by the sensory neuron as a result of repeated activation of an AP. This repeated activation reduces the influx of calcium ions (Ca++) into the axon terminals of sensory neurons. Ca++ is responsible for mobilizing the vesicles that store neurotransmitter molecules toward the presynaptic membrane, where glutamate is released into the synapse. Therefore, short-term habituation of the GWR in Aplysia is mainly a presynaptic phenomenon.
