A learned association of taste with visceral distress

Farmers know, probably from the dawn of farming, that animals tend to avoid poisonous bait if they survive their first encounter with it. The farmers themselves may have probably noticed that foodstuff comes to evoke disgust if consuming it results in nausea and intestinal distress. However, common knowledge does not always penetrate academic barriers: it has taken John Garcia and his colleagues several distressful years to convince the referees of respectable scientific journals that conditioned taste aversion (CTA) does occur (Garcia 1981). This almost became a case of CSA (conditioned submission aversion).

Also dubbed the Garcia Effect, Bait Shyness, or the Béarnaise Sauce Effect (many a reader can probably offer idiosyncratic terms based on unpleasant personal experience), CTA does differ in a critical parameter from other "associative learning "paradigms. This parameter is the interstimulus interval (ISI), i.e. the time interval between the conditioned (CS) and the unconditioned (US) "stimuli. Whereas in "classical and "instrumental conditioning an ISI of more than seconds commonly renders training ineffective, CTA training tolerates an ISI of several hours. It is this deviation from the widely accepted paradigm, namely that two stimuli must come close together in time in order to become associated in mind, that has led respectable psychologists to doubt the early scientific accounts of CTA.

The first systematic studies of CTA were reported by Rzoska (1953) and by Garcia et al. (1955). Both conducted their experiments on the "rat. Rzoska investigated the effect of poisoned bait on the subsequent rejection of the same bait; Garcia noticed that the association of a saccharin solution with exposure to y-irradiation, which induces malaise, suppresses subsequent consumption of saccharin. He later produced CTA by associating the saccharin with the delayed injection of malaise-inducing compounds (Garcia et al. 1966). Saccharin is used to this day as a standard CS in CTA experiments. Many other tastes can be used as well; they are most effective if unfamiliar to the "subject at the time of conditioning (Revusky and Bedarf 1967). The US could also vary, from rotation and irradiation to drugs and poisons. A standard US is an intraperitoneal (i.p.) injection of a LiCl solution, which produces transient visceral distress within a few minutes of injection. In a commonly used protocol, the rat (or mouse) is made slightly thirsty, and then given to drink the diluted taste solution for 10-20 min. This is followed after 1-3 h by the US. A few days later, the "subject is tested for taste avoidance, either by presenting it with the CS only (single-bottle test), or by permitting it to choose between the CS and another 'innocent' tastant (multiple-bottle test).

On the one hand, the ISI in CTA can extend up to 6-8 h, but, on the other, it cannot be made too short: 10s only is ineffective (Schafe et al. 1995). It seems that the brain has an "a priori tendency to distinguish ingestion-induced malaise, which requires at least several minutes to develop, from other types of negative "reinforcers. Similarly, stimuli that act on non-visceral receptors and have less intimate association with food, such as tones, visual "cues, or cutaneous pain, although very effective in classical and instrumental conditioning, are ineffective in CTA (Garcia et al. 1968). Odours can be used as CS in long delay conditioning (Slotnick et al. 1997), but are less effective, and work best when associated with taste ('taste potentiated odour aversion', TPOA; Rusiniak et al. 1979).

CTA offers significant advantages for the investigation of the phenomena and mechanisms of simple associative learning. The single-trial "acquisition facilitates the correlation of neuronal events with learning, and targeted interventions in the process by drugs or other treatments ("criterion, "method). The CTA protocol is highly reproducible and the resulting memory is long lasting, which permits analysis of multiple memory phases. The extended ISI enables the dissociation of the CS acquisition from the CS-US association. And since rodents are involved, a multi"level analysis of learning and memory, from the behaviour to the molecules and back, is feasible. CTA has therefore become a popular "assay and "paradigm in memory research. Whereas the behavioural parameters of CTA have been described in detail (Bures et al. 1988, 1998), less is known about the brain circuits that subserve this behaviour. It is generally accepted that the gustatory area in the insular "cortex plays a part in processing the detection of taste unfamil-iarity and in encoding the taste "representation; the parabrachial nucleus is involved in the association of the taste with the malaise; and the "amygdala subserves the hedonic assessment of the taste, as well as the integration and expression of CTA (Figure 17)

Vpm Rat Brain

Fig.17 (a) A scheme of the central taste system in the rat, which mediates CTA learning. VII, IX, X—cranial nerves;Am, *amygdala; CGA, the central gustatory area in the insular *cortex; LH, lateral hypothalamus; NTS, the nucleus of the solitary tract in the brainstem; PBN, the parabrachial nucleus in the pons; VPM, the ventroposteriomedial nucleus of the thalamus, which contains the thalamic taste area(s). The CGA is involved in detection of taste familiarity and in the taste memory; the amygdala in encoding the hedonic valence of the taste and in the acquisition and performance of CTA; and the PBN particularly in the association of the CS with US in CTA. (b) Rats injected i.p. with LiCl an hour after consuming an unfamiliar solution of saccharin display high aversion toward saccharin when tested 3 days later. The test involves a choice between saccharin and water; 0.5 means equal preference, and a low score means preference of saccharin. It can be seen that rats injected in training with NaCl, which does not induce malaise (*control), come to prefer the saccharin to water.

LiCI NaCI

Fig.17 (a) A scheme of the central taste system in the rat, which mediates CTA learning. VII, IX, X—cranial nerves;Am, *amygdala; CGA, the central gustatory area in the insular *cortex; LH, lateral hypothalamus; NTS, the nucleus of the solitary tract in the brainstem; PBN, the parabrachial nucleus in the pons; VPM, the ventroposteriomedial nucleus of the thalamus, which contains the thalamic taste area(s). The CGA is involved in detection of taste familiarity and in the taste memory; the amygdala in encoding the hedonic valence of the taste and in the acquisition and performance of CTA; and the PBN particularly in the association of the CS with US in CTA. (b) Rats injected i.p. with LiCl an hour after consuming an unfamiliar solution of saccharin display high aversion toward saccharin when tested 3 days later. The test involves a choice between saccharin and water; 0.5 means equal preference, and a low score means preference of saccharin. It can be seen that rats injected in training with NaCl, which does not induce malaise (*control), come to prefer the saccharin to water.

(Yamamoto et al. 1994; Bures et al. 1998; Lamprecht and Dudai 2000).

It is unlikely that the tolerance of CTA training to long ISI stems from unique types of molecular "coincidence detectors in the central taste circuit. Information gathered so far indicates that the molecular mechanisms that subserve CTA are similar to those that subserve other forms of learning, such as the activation of "glutamate and "acetylcholine receptors and the modulation of "immediate early gene expression (Lamprecht et al. 1997; Rosenblum et al. 1997; Berman et al. 1998, 2000; Gutierrez et al. 1999). Probably, the tolerance to long delays results from special circuit properties, shaped in evolution to ensure 'prepared learning' ("a priori) of the avoidance of food toxins (e.g. Shipley and Sanders 1982). An appealing hypothesis is that sampling a taste, especially an unfamiliar one, creates an 'active' ("taxonomy), short-term memory trace in the gustatory cortex, and possibly in some other stations in the central taste pathway (Figure 17). This memory of the CS lasts for only a few hours and is accessed by stations in the central taste circuit that can also detect malaise. Candidate mechanisms that could encode this type of memory are the "persistent phosphorylation of synaptic proteins (Rosenblum et al. 1997; "protein kinase), local "protein synthesis, and other types of tagging of the active synapses (Frey and Morris 1997; "consolidation). If malaise is sensed while the short-term taste memory is still active, the CS and the US information converge, probably in the parabrachial nucleus and possibly also in the amygdala. This in turn triggers the cellular mechanisms that register the long-lasting taste-malaise association.

Selected associations: A Priori, Associative learning, Classical conditioning, Paradigm, Surprise

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