The gradual diminution of the response to a stimulus following the repeated presentation of the same or a similar stimulus

Habituation is commonly classified as a type of non"associative learning ("taxonomy). This is because it is assumed to be governed solely by the parameters of the habituated, unconditioned stimulus, in the absence of associations with other stimuli. This assumption may be wrong. It is questionable whether any type of learning is indeed purely nonassociative. In habituation, associations are formed with the "context (Wagner 1979; Marlin and Miller 1981; Rankin 2000), and possibly also with "palimpsests of the "internal representation, accumulated over the individual's history. Another common myth concerning habit-uation is that because it involves a diminution of response, no new information is acquired. On the contrary: that a certain stimulus can be safely ignored is in itself new valuable information, which promotes adaptation to the milieu and prevents superfluous defensive reflexes. Kandel (1976) cites a fable by Aesop, which epitomizes this point: 'A fox, who had never yet seen a turtle, when he fell in with him for the first time in the forest was so frightened that he was near dying with fear. On his meeting with him for the second time, he was still much alarmed but not to the same extent as the first. On seeing him for the third time, he was so increased in boldness that he went up to him and commenced a familiar conversation with him.' Be it a fox or a turtle, a spider (in which it was first described in the scientific literature; Peckham and Peckham 1887), a scientist or a mollusc—habituation is part of the behavioural repertoire of all the cellular organisms analysed so far (Christoffersen 1997), including unicellular organisms and even cells in culture (McFadden and Koshland 1990). From the point of view of the neurosciences, however, there is some advantage in focusing on habituation in organisms that do contain a nervous system.

'Habituation' is a central nervous system process. Use-dependent response decrements that occur because of sensory and peripheral processes, are termed 'adaptation'. Although clearly not a unitary process, several attributes "generalize over many instances of habituation (Thompson and Spencer 1966; Staddon and Higa 1996). These include, among others:

1. Stimulus specificity. Habituation to one stimulus does not usually generalize to other stimuli. This distinguishes habituation from response decrements due to adaptation, fatigue, or disease.

2. Intensity sensitivity. Commonly, the weaker the habituating stimulus, the more rapid or pronounced is habituation.

3. Rate sensitivity. The rate of formation, robustness and "persistence of habituation is a function of the time between the presentations of the stimulus (interstimulus interval, ISI). Habituation is faster when the ISI is short, and more persistent, once achieved, when the ISI is long; the dependence on ISI could, however, be rather tricky (e.g. Davis 1970).

4. Spontaneous recovery. Withholding the habituating stimulus commonly results in time-dependent recovery of the response. Recovery is faster if the ISI in habituation training is kept short (see 3 above). Repeated cycles of habituation and spontaneous recovery result in progressively greater habituation.

5. Undershooting. Habituation may proceed below the naive response level.

6. Dishabituation. The presentation of another (usually noxious) stimulus results in the recovery of the habituated response.

Not all the above parameters are satisfied in every "system that habituates. Dishabituation is considered the most critical "criterion, and is commonly employed to establish that habituation has indeed occurred. Dishabituation resembles "sensitization, which is the facilitation of a nonhabituated response; cellular, circuit, behavioural, and developmental studies have, however, indicated that habituation and sensitization differ in multiple parameters (Rankin and Carew 1988; Byrne and Kandel 1996; Hawkins et al. 1998). Is dishabituation only a disruption or removal of habituation (Dodge 1923), or is it an independent process superimposed on habituation (Grether 1938)? Habituation and dishabituation could be shown to have different intrinsic time courses. This supports the idea that they are independent processes that interact to yield the final behavioural outcome ('the dual-trace hypothesis'; Groves and Thompson 1970). Multiple interpretations and functional "models of habituation have been proposed over the years (Coombs 1938; Sharpless and Jasper 1956; Sokolov 1963a,b; Glaser 1966; Konorski 1967; Wagner 1979; Staddon and Higa 1996). A useful classification distinguishes 'feedback' from 'feedforward' models (Staddon and Higa 1996). In 'feedback' models the response is inhibited by the "percept or the immediate memory of the current stimulus. In 'feed-forward' models the integrated longer-term memory of past stimuli is fed forward to dampen the immediate effect of the current stimulus. It is unlikely that any single type of model will generalize to all habituating systems, from the simplest to the complex.

The cellular bases of habituation have been pursued in a number of experimental preparations. Noteworthy among these are the cat spinal reflexes (Spencer et al. 1966); the rat acoustic startle reflex (Davis 1970; Jordan and Leaton 1983; "fear conditioning); and the "Aplysia defensive reflexes (Kandel 1976; Frost et al. 1997; Hawkins et al. 1998). The studies of short- and long-term forms of habituation in Aplysia epitomize a comprehensive reductionist research programme, in which the combination of reductive and simplifying steps (Dudai 1989; "reduction) resulted in the identification of circuit, "synaptic, and molecular correlates of habit-uation. Interestingly, although considered the simplest of all types of learning, the cellular and molecular analysis of habituation in Aplysia has so far yielded less elaborate mechanistic models than the analysis of sensitization or "classical conditioning in the same organism. The major conclusion was that habituation is due to homosynaptic1 depression of the monosynaptic sensory-motoneuron connection that mediates the reflex (Fig. 5, page 16). The process involves "inactivation of "calcium channels and depletion of releasable "neurotransmitter molecules (Frost et al. 1997). In the long term, morphology is altered as well, and there is a reduction in the frequency and size of the active zones in the synapse (Bailey and Chen 1983). All this portrays habituation as use-dependent modification confined to the elementary, minimal reflex pathway. In real life, the habituated response is more likely to be subserved by heterosynaptic processes in polysynaptic pathways as well (Hawkins et al. 1998). Habituation has been reported to involve modulation of pathways that are extrinsic to the minimal reflex pathways in another "simple system, the escape response of the crayfish (Krasne and Teshiba 1995). As expected, multiple pathways are also involved in the habituation of more complex behaviours, such as the orienting reflex in mammals (Kwon et al. 1990).

The cellular analysis of habituation could serve to illustrate the problematics of "level shifts in a reductive research programme. Suppose you are interested in the neuronal mechanisms of habituation, have just decided to go cellular, and started to record the response of neurons in the visual cortex of the "monkey. You find a response decrement with repetitive presentation of the same or similar stimuli ('repetition suppression', Desimone 1996). Furthermore, if you present a novel, "surprising stimulus, the response will recover. Is this the cellular analogue of behavioural habituation? Well, probably not. It may actually subserve "priming, which is facilitation of the behavioural response. Or it might also be the cellular correlate of "recognition, resulting in an enhanced rather than a diminished behavioural

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Fig. 33 Simple habituation: the worm Nereis contracts in response to a mechanical shock (full circles) or a moving shadow (open circles). The response habituates readily. Habituation to one type of stimulus is independent of habituation to the other type.This is different from the response decrement due to fatigue, which *generalizes over types of stimuli. Interstimulus interval = 1 min. (Adapted from Clark 1960.)

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Fig. 33 Simple habituation: the worm Nereis contracts in response to a mechanical shock (full circles) or a moving shadow (open circles). The response habituates readily. Habituation to one type of stimulus is independent of habituation to the other type.This is different from the response decrement due to fatigue, which *generalizes over types of stimuli. Interstimulus interval = 1 min. (Adapted from Clark 1960.)

response. Hence habituation of cellular response may subserve a facilitatory behavioural response, and similarly, facilitation of the cellular response may end up in a decremental behavioural response.2 The take-home message: the contribution of neuronal "plasticity to behavioural plasticity does not necessarily honour "Ockham's razor.

Selected associations: Context, Cue, Plasticity, Recognition, Sensitization

1A process is called 'homosynaptic' if it involves only the modulated synapse, and 'heterosynaptic' if it involves modulatory interneurons.A pathway is 'monosynaptic' if it involves only a single synaptic connection, and 'polysynaptic' if it involves multiple synaptic connections. 2The relationship of habituation to some other types of use-dependent modification in response is intricate. Priming is an example. Habituation could be regarded as a type of gradual negative priming. Indeed in an influential model of habituation, the decremental behavioural response is formulated in terms of variations in stimulus processing that depend on whether or not the representation of the stimulus, or its associations, has been primed (Wagner 1979). Recognition is another example. Suppose in a recognition paradigm the subject stops responding because the stimulus is recognized as familiar—Is this habituation to the stimulus? Yet for habituation to occur, recognition of the stimulus is a must. In this example the 'recognition' terminology will always be preferred in mammals when the mediotemporal lobe is involved.

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