Kenneth W. Rusiniak

Flavor-illness aversions: potentiation of odor by taste in rats

For the Sprague–Dawley rat, the odor of almond-scented water proved to be a weak cue for lithium chloride-induced illness, while the taste of saccharin water was very effective. However, when the weak almond color was combined with the strong saccharin taste into a compound cue and followed by lithium chloride-induced illness in a compound conditioning paradigm, taste strongly potentiated odor. Before illness, rats were hesitant (neophobic) to consume almond-scented saccharin solutions. During extinction tests conducted after the compound solution was paired with illness, rats displayed a stronger aversion to the odor component than to the taste component. Aversions for the odor component increased in direct proportion to the concentration of the taste component that was present only on the conditioning trial. Tests with anosmic rats indicated that almond-scented tap water was primarily an olfactory cue having little if any taste component. In contrast, when the almond odor was combined with saccharin taste in a second-order conditioning paradigm, rats did not use odor to avoid taste previously made aversive by illness; nor did they acquire aversions for taste paired with aversive odor. Synergistic potentiation of aversions for the weak stimulus component by the strong component contrasts with the interference effects usually observed in classical conditioning. Taste may index the memory for distal poison cues when toxicosis is delayed after ingesting poison to circumvent interference by intervening cues. This allows the animal to form selectively an aversion for distal poison cues, thus reducing the risk of tasting poison.

Coyote Predation Control by Aversive Conditioning

Conditioned aversions were induced in coyotes by producing lithium chloride illness in them following a meal, and the effects upon eating and attack behavior were observed. One trial with a given meat and lithium is sufficient to establish a strong aversion which inhibits eating the flesh of that prey. One or two trials with a given flesh (lamb or rabbit) specifically suppresses the attack upon the averted prey but leaves the coyote free to attack the alternative prey. A method of saving both prey and predator is discussed.

Flavor—illness aversions: Potentiation of odor by taste is disrupted by application of novocaine into amygdala

Taste and odor have different properties in toxiphobic conditioning. When each is used alone, taste becomes aversive when followed by immediate or delayed poison, while odor becomes aversive only if followed by immediate poison. However, if odor and taste are presented as a compound and followed by delayed poison, then odor does become aversive when tested alone. It is as if taste has potentiated the odor signal. Several experiments assessed the role of the amygdala in this potentiation effect by anesthetizing the amygdala with 10% novocaine. Novocaine applied 30 min before presentation (Pre-CS) of an odor-taste compound disrupted the potentiated odor aversion but not the taste aversion. In contrast, novocaine applied 1 min after the compound odor-taste or 1 min prior to LiCl poison did not dissociate odor and taste aversions; both odor and taste aversions were facilitated. Novocaine applied 30 min before an odor alone also disrupted an odor aversion induced by immediate LiCl. But identical treatment did not disrupt odor avoidance conditioned by immediate foot-shock, suggesting that amygdala anesthesia does not simply produce anosmia. Pre-CS novocaine treatment also disrupted flavor neophobia prior to conditioning. The results suggest that novocaine applied to the amygdala disrupts the integration of odor with taste and illness during toxiphobic conditioning.

Cortical lesions: flavor illness and noise-shock conditioning

We studied the effects of neocortical lesions in rats upon (a) aversive conditioning where a flavor is paired with a subsequent illness, and (b) aversive conditioning where a noise is followed by a foot shock. Lesions of the anterior cortex produced deficits in both paradigms, regardless of whether the gustatory cortex was damaged or spared. Lesion size was more important than location for taste aversion acquisition. Gustatory cortical lesions, as well as other cortical lesions, produced “intersession memory” deficits between training days in the noise-shock paradigm. Within sessions, the acquisition slopes were similar for control and lesioned rats. These data favor a general learning effect for any anterior cortical lesion rather than a specific effect of gustatory lesions on flavor-illness conditioning.

Prey-lithium aversions. II: laboratory rats and ferrets

Lithium-induced prey aversions were studied in the laboratory rat and ferret. Both species acquired aversions, blocking consumption of flavored foods and the flesh of mice. In the rat, attack was also blocked when illness immediately followed mouse-killing, when mice were dipped in a strongly aversive flavor, and when illness followed killing and eating of prey dipped in an artificial flavor with strong olfactory and gustatory properties. Testing context was of some importance. The ferret, on the other hand, continued to attack, killing mice with its feet rather than with a bite to the neck. Strong footshock produced a transient inhibition of attack that was specific to the training situation. These results with laboratory species are in distinct contrast to those with wild predators.

Dissociation of odor and taste in shock-avoidance learning.

Intact rats effectively utilized the odor cf apple juice to avoid shock but did not acquire an aversion when this odor was followed by illness. In contrast, anosmic rats did not effectively utilize the taste of apple juice to avoid shock, but did acquire an aversion when this taste was followed by illness. A weak saccharin solution was not an effective cue for shock avoidance in intact rats, but when the concentration was increased fourfold so as to produce an odor, the saccharin solution became an effective shock signal in both active and passive avoidance. Increased saccharin concentration was a less effective cue for anosmic rats, but when coupled with intense shock, learning was evidenced. Olfactory bulbectomy had a more profound effect upon performance than mere anosmia. Learning theorists should recognize: (1) That odor, unlike taste, primarily functions as an exteroceptive cue. (2) Each afferent channel has a unique behavioral function which determines the parameters for conditioning and the topography of conditioned responses. (3) These unique functions are related to the central projections of afferent channels and to evolutionary species history.

Ethanol-induced flavor aversions in rats with subdiaphragmatic vagotomies.

In two experiments rats with subdiaphragmatic vagotomies were compared to sham-operated rats in the acquisition and extinction of a flavor aversion with ethanol as the illness-inducing agent. Vagotomized rats developed aversions equivalent to those of sham-operated rats whether the ethanol was administered intragastrically (Experiment 1) or intraperitoneally (Experiment 2). Because vagotomy eliminates the majority of sensory input from the gastrointestinal tract, ethanol must exert its aversive effects as a blood-borne toxin rather than as a gastrointestinal irritant.

The Neural Integration of Feeding and Drinking Habits

For the rat, the interaction of food-related cues and the visceral feedback following ingestion largely determines future consummatory behavior. In early work (Garcia & Koelling, 1966), it was shown that taste cues were most readily associated with illness; conditioned taste aversions were formed after only a single taste-illness experience. Unlike most other demonstrations of classical conditioning, the delay between the taste conditioned stimulus (CS) and the illness unconditioned stimulus (US) could be an hour or more and strong taste aversions still would be formed. In contrast to tastes, an audio-visual signal was a poor CS for illness conditioning, acquiring little or no aversive properties following a single toxic US. If footshock was used as a US, the converse obtained. An audio-visual CS was readily associated with footshock US whereas taste was a poor CS in shock avoidance conditioning.

Developmental flavor experience affects utilization of odor, not taste in toxiphobic conditioning.

Feeding experiences were varied in developing rats and the effects upon flavor neophobia and lithium chloride-induced flavor aversions were observed. In Experiment 1, nursing experience of neonate rats was reduced by artificial feeding via intragastric cannula; the rats then were tested with apple juice paired with lithium chloride injection at weaning or maturity. Conditioned aversions were not affected, but neophobia to novel apple juice was attenuated in artificially-reared rats tested at maturity. In Experiment 2, rats received enriched feeding experience after weaning, which consisted of (a) obtaining many complex flavors, a few of which were paired with poisoning, effortlessly in the home cage, or (b) foraging for various foods on an elevated maze. No dramatic effects on neophobia or conditioned taste aversion for saccharin water were apparent. In Experiment 3, rats were given experience after weaning with vanilla-scented water either paired or unpaired with quinine water, and then tested with the odor of almond or that odor compounded with saccharin water for neophobia and lithium-induced aversions. Flavor-experienced rats exhibited more pronounced odor conditioning and more resistance to extinction of the odor aversion after both simple and compound conditioning. In contrast, saccharin taste aversions were relatively unchanged. Apparently, enriched feeding and drinking experience facilitates the utilization of odor more than taste cues.

Visceral Feedback and the Taste Signal

Visceral feedback after eating a meal modifies the taste of the food and drink by psychological processes which are of special interest to students of biofeedback. For simplicity, consider an unlimited amount of a tasty fluid placed before a hungry subject. The taste of the fluid is the perceptual signal, ingestion is the process to be controlled and homeostatic well-being is the state to be achieved. If the fluid is a creamy substance, rich in calories, it tastes delicious at the beginning of the meal and the subject drinks heartily. As the caloric mass accumulates in the gut, satiety is achieved before tissue needs are redressed, as if the viscera has sensing devices which accurately estimate the amount of food needed to achieve the ultimate homeostatic balance (Novin, 1976; Schachter, 1971; McHugh, Moran, & Barton, 1975).