Provenza (1995) has proposed that there are three kinds of memory involved in the association between sensory and metabolic properties of foods. The first is that provided by evolution through the special and general senses, whereby some food-related stimuli are innately aversive (e.g. odour of faeces) or preferred (e.g. sweet taste). The second kind of memory is provided by the mother, who is a source of ‘transgenerational knowledge’, reducing the risk involved in learning about foods and environments. The third kind of memory is that of the individual itself, involving post-ingestive feedback from nutrients and toxins and associations with sensory properties of foods. Thus, each animal has its own genetic and behavioural history, making it difficult to predict how it will react in a particular choice situation.
CS–US interval
For most associations to be learned, the CS (the ringing of a bell in the case of Pavlov’s dog) must be presented a few seconds before the US (the presentation of food in order to elicit salivation). However, with learned preferences and aversions to foods, the presentation of the conditioning stimulus (CS, the flavour/appearance of the food that the animal has learned to be associated with its metabolic properties) and of the unconditioned stimulus (US, the effects of the metabolites absorbed from the food) can be many minutes, or even hours, apart.
In some cases animals find a food aversive only when discomfort is felt soon after ingesting that food. For example, giving sheep 150 mg/kg LiCl (US) either at the time of offering oat chaff (CS) or 1 or 2 h later resulted only in the development of an aversion for that food in those given LiCl at the time of offering the chaff. In other cases, however, longer intervals can elapse between CS and US, such as at least 8 h in sheep (Arsenoset al., 2000). Preferences are stronger, however, when the interval is short (Villalba et al., 1999), and this
may well be why a stronger preference is induced by starch (rapidly digested) than a fibrous material when introduced into the rumen, and why sheep actively seek plant parts high in soluble carbohydrates.
It is not even necessary for animals to be conscious during the time they are exposed to the nauseating effects of a toxin: when sheep were given a novel food and then anaesthetized while a nauseating dose of LiCl was administered, and maintained unconscious until its effects had dissipated, they still found that food aversive when offered it subsequently (Provenza et al., 1994a, b). Thus, animals need not be consciously aware that some foods are mildly toxic and are inducing a learned aversion; the whole process is automatic unless, of course, the toxin concerned is powerful, in which case the discomfort is obvious.
Speed of learning
It is to be expected that the speed of learning will depend on the degree to which the animal has been moved from its normal state, e.g. by previous feeding of a deficient diet, as the reinforcing properties of feeding can be very rapid indeed.
The speed with which chicks learned new associations between the protein content of a food and its colour was investigated by training them to associate one colour with a high protein content of 248 g/kg and another colour with a low protein content of 103 g/kg (Hannah, 2001). Then they were fasted for 1 h, offered both foods and the time taken to start eating from each was monitored. In Fig. 6.6, the area to the left of the dashed vertical lines shows that they ‘attacked’ the high-protein food significantly more quickly than the low-protein food, whether the high- or the low-protein food was coloured green. On day 48, the colours were reversed and there was a rapid reversal of the attack times so that within 3 days the high-protein food was once again
0 50 100 150 200 250 300
40 45 50 55
Age (days) (a)
0 50 100 150 200 250 300
40 45 50 55
Age (days) (b)
Attack time (s) Attack time (s)
Fig. 6.6. Mean times to attack foods with different protein contents and colours. (a) treatment 2 (red, HP, green, LP and reversed at day 48); (b) treatment 4 (red, LP, green, HP and reversed at day 48). 䡲, red food; ●, green food; the vertical dashed line shows the time that the food colours were reversed (from Hannah, 2001).
being attacked far more quickly than the low-protein food. This relearning time is similar to those noted in other experiments with chicks.
Jones and Forbes (1984) found that sheep which obviously discriminated against quinine-treated hay in a preliminary period ate equal amounts of treated and untreated hay in subsequent 5-day choice periods, thereby demonstrating adaptation as they learned that there were no harmful consequences to eating the quinine-flavoured food. Following a change in flavour, even without changes in the nutritive value of food, sheep sample the food cautiously.
Speed of forgetting
There is a difference between a situation in which the UC–CS association is changed, as in the examples above, and one in which an association is no longer reinforced. In other words, once learned, for how long is the memory of the nutritive value of a food retained? The answer seems to vary with the circumstances. This makes sense because it is necessary, on the one hand, for conditioned taste aversions to persist (otherwise they have no function), but also to be flexible (otherwise an animal might be saddled with an unnecessary aversion for the rest of its life). The stronger the aversion the longer it persists.
Growing broilers seem to forget the aversive properties of a coloured food paired with an i.p. injection of cholecystokinin within a few days (see Fig. 6.2) and it might be thought, therefore, that this aversion is a mild one. However, it needs to be remembered that the younger an animal, the faster it is likely to learn and forget. Once sheep have eaten > 10 g of supplement/day they will subsequently eat it readily even if they have not seen it for 3 years. Sheep moved from native pastures to high-quality pasture select a food with significantly lower nitrogen content than sheep reared from birth on that pasture. This is true even after the introduced sheep have been on the good pasture for 3 months.
There are many examples to show that experience of eating a particular food is helpful. Sheep reared on grass are more dextrous and have a higher biting rate for grass than those experienced in harvesting shrubs. Conversely, those used to eating shrubs do so more efficiently than those with only grass experience. Goats with experience of browsing blackbrush eat faster and more by breaking twigs off than do inexperienced goats. Lambs with experience of grazing the serviceberry shrub later grazed it more efficiently when it was sparse than did naïve lambs, while there was no such difference in the rate of eating of other foods. Lambs or ewes recognized foods to which LiCl had previously been added, after 2 months without exposure.
If an animal learns that a food item is unpalatable and avoids it, does it forget the unpalatability by it not being reinforced? Do unreinforced encounters have a memory-jogging effect? Usually animals sample from time to time foods to which they are averse, presumably so that they can be made aware of any change in their properties.