Neuronal representation of conditioned taste in the basolateral amygdala of rats

Animals develop robust learning and long lasting taste aversion memory once they experience a new taste that is followed by visceral discomfort. A large body of literature has supported the hypothesis that basolateral amygdala (BLA) plays a critical role in the acquisition and extinction of such conditioned taste aversions (CTA). Despite the evidence that BLA is crucially engaged during CTA training, it is unclear how BLA neural activity represents the conditioned tastes. Here, we incorporated a modified behavioral paradigm suitable for single unit study, one which utilizes a sequence of pulsed saccharin and water infusion via intraoral cannulae. After conditioning, we investigated BLA unit activity while animals experience the conditioned taste (saccharin). Behavioral tests of taste reactivity confirmed that the utilized training procedure produced reliable acquisition and expression of the aversion throughout test sessions. When neural activity was compared between saccharin and water trials, half of the recorded BLA units (77/149) showed differential activity according to the types of solution. 76% of those cells (29/38) in the conditioned group showed suppressed activity, while only 44% of taste reactive cells (17/39) in controls showed suppressed activity during saccharin trials (relative to water trials). In addition, the overall excitability of BLA units was increased as shown by altered characteristics of burst activity after conditioning. The changes in BLA activity as a consequence of CTA were maintained throughout test sessions, consistent with the behavioral study. The current study suggests that the neuronal activity evoked by a sweet taste is altered as a consequence of CTA learning, and that the overall change might be related to the learning induced negative affect.     

Social interaction modifies learned aversions, sodium appetite, and both palatability and handling-time induced dietary preference in rats (Rattus norvegicus)

In a series of four experiments, I examined the extent to which socially transmitted diet preference could counteract the effects of a learned aversion (Experiment 1), a palatability-based diet preference (Experiment 2), a polyethylene glycol 20,000-induced sodium appetite (Experiment 3), and a handling-time induced dietary preference (Experiment 4). I found that rats poisoned after eating a novel diet ate very substantial amounts of the averted diet following interaction with conspecifics that had eaten the averted diet. Following interaction with conspecifics that had eaten an unpalatable diet, rats offered a choice between palatable and unpalatable diets ate more than twice as much unpalatable diet as did controls lacking social experience. Sodium-deficient rats offered a choice between sodium-enriched and sodium-adequate diets ate less than half as much sodium-enriched diet, following interaction with conspecifics that had eaten sodium-adequate diet as did control rats lacking social experience. Rats offered a choice between isocaloric, roughly equipalatable foods with long and short handling times (e.g., sunflower seeds with and without shells) chose the food having the longer handling time after interacting with conspecifics eating that food. These findings suggest that social influence is a major factor in guiding diet selection by rats.     

Effect of preconditioning unconditioned stimulus experience on learned taste aversions.

One taste-aversion study using male Long-Evans rats in which ethanol was the unconditioned stimulus (UCS) and six studies in which lithium chloride (LiCl) was the UCS demonstrate that (a) exposure to the UCS prior to conditioning retards subsequent acquisition of learned taste aversions; (b) a single preconditioning UCS exposure is sufficient to attenuate conditioning; (c) the preconditioning UCS exposure must occur within a limited period prior to conditioning to attenuate learning; (d) repeated conditioning trials will override the effect of prior exposure to the UCS; (e) tolerance to the UCS is not a necessary condition for the attenuation effect to occur; (f) pairing the preconditioning UCS with a novel flavor other than the CS does not remove the preexposure effect, although it may reduce its magnitude; and (g) the degree of disruption is a positive function of preconditioning UCS dosage and an inverse function of conditioning UCS dosage.     

Role of illness in producing learned taste aversions in rats: a comparison of several rodenticides.

Several toxic agents were compared in order to test the effect of various types of illness in producing learned taste aversions. After a 10-min sucrose drinking trial, groups of rats were injected intraperitoneally with lithium chloride or with a strong, near lethal dose of a rodenticide. Strong sucrose aversions were acquired by groups injected with lithium chloride, copper sulfate, sodium fluoroacetate, or red squill, and very weak or no aversions were learned by groups injected with thallium, warfarin cyanide, or strychnine. The results were discussed in terms of onset of symptoms, duration of symptoms, and kinds of physiological effects necessary to produce aversions. It was concluded that the effects of different drugs may be mediated by different physiological systems learned taste aversions.     

Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats

Lesions of the basolateral amygdala (BLA) have long been associated with abnormalities of taste-related behaviors and with failure in a variety of taste- and odor-related learning paradigms, including taste-potentiated odor aversion, conditioned taste preference, and conditioned taste aversion. Still, the general role of the amygdala in chemosensory learning remains somewhat controversial. In particular, it has been suggested that the amygdala may not be involved in a form of chemosensory learning that has recently received a substantial amount of study-socially transmitted food preference (STFP). Here, we provide evidence for this involvement by pharmacologically inactivating the basolateral amygdala bilaterally during STFP training. The same inactivation sites that impaired taste aversion learning eliminated the normally conditioned preference for a food smelled on a conspecific's breath. Impairments of learned preference persisted even in testing sessions in which BLA was not inactivated, and learning was normal when the BLA was inactivated only during testing sessions; thus, the impairment was a true acquisition deficit. In conjunction with previous results from other paradigms, therefore, our data suggest that the amygdala is vital for learning procedures involving pairings of potent and arbitrary chemosensory stimuli.     

Dissociable effects of basolateral amygdala lesions on decision making biases in rats when loss or gain is emphasized

Individuals switch from risk seeking to risk aversion when mathematically identical options are described in terms of loss versus gains, as exemplified in the reflection and framing effects. Determining the neurobiology underlying such cognitive biases could inform our understanding of decision making in health and disease. Although reports vary, data using human subjects have implicated the amygdala in such biases. Animal models enable more detailed investigation of neurobiological mechanisms. We therefore tested whether basolateral amygdala (BLA) lesions would affect risk preference for gains or losses in rats. Choices in both paradigms were always between options of equal expected value—a guaranteed outcome, or the 50:50 chance of double or nothing. In the loss-chasing task, most rats exhibited strong risk seeking preferences, gambling at the risk of incurring double the penalty, regardless of the size of the guaranteed loss. In the betting task, the majority of animals were equivocal in their choice, irrespective of bet size; however, a wager-sensitive subgroup progressively shifted away from the uncertain option as the bet size increased, which is reminiscent of risk aversion. BLA lesions increased preference for the smaller guaranteed loss in the loss-chasing task, without affecting choice on the betting task, which is indicative of reduced risk seeking for losses, but intact risk aversion for gains. These data support the hypothesis that the amygdala plays a more prominent role in choice biases related to losses. Given the importance of the amygdala in representing negative affect, the aversive emotional reaction to loss, rather than aberrant estimations of probability or loss magnitude, may underlie risk seeking for losses.     

Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala

It is well established that glucocorticoid hormones strengthen the consolidation of hippocampus-dependent spatial and contextual memory. The present experiments investigated glucocorticoid effects on the long-term formation of conditioned taste aversion (CTA), an associative learning task that does not depend critically on hippocampal function. Corticosterone (1.0 or 3.0 mg/kg) administered subcutaneously to male Sprague–Dawley rats immediately after the pairing of saccharin consumption with the visceral malaise-inducing agent lithium chloride (LiCl) dose-dependently increased aversion to the saccharin taste on a 96-h retention test trial. In a second experiment, rats received corticosterone either immediately after saccharin consumption or after the LiCl injection, when both stimuli were separated by a 3-h time interval, to investigate whether corticosterone enhances memory of the gustatory or visceral stimulus presentation. Consistent with the finding that the LiCl injection, but not saccharin consumption, increases endogenous corticosterone levels, corticosterone selectively enhanced CTA memory when administered after the LiCl injection. Suppression of this training-induced release of corticosterone with the synthesis-inhibitor metyrapone (35 mg/kg) impaired CTA memory, and was dose-dependently reversed by post-training supplementation of corticosterone. Moreover, direct post-training infusions of corticosterone into the insular cortex or basolateral complex of the amygdala, two brain regions that are critically involved in the acquisition and consolidation of CTA, also enhanced CTA retention, whereas post-training infusions into the dorsal hippocampus were ineffective. These findings provide evidence that glucocorticoid effects on memory consolidation are not limited to hippocampus-dependent spatial/contextual information, but that these hormones also modulate memory consolidation of discrete-cue associative learning via actions in other brain regions.     

Formation of taste aversions in rats following prior exposure to sickness

Findings from the present experiments extend those of earlier studies and show that rats form weaker conditioned taste aversions if they are exposed to a sickness-inducing agent prior to a single training trial. The present experiments appear to rule out the possible confounding factors that, during pretraining, (1) animals became addicted to the drugs that were intended to induce sickness during training, (2) drug tolerances were created and hence reduced the effectiveness of the same or different sickness-inducing agents used to induce sickness during training, or (3) associations between other stimuli and sickness were formed and interfered with or blocked the formation of subsequent taste aversions. It was concluded that the associative capacity of sickness can be reduced through pre-exposure.     

Time of day-dependent latent inhibition of conditioned taste aversions in rats

We have determined that the temporal context of drinking can modulate latent inhibition of learned saline aversions in Wistar rats by changing the time of day of drinking of the preexposure and conditioning phases. Latent inhibition was absent in the group preexposed and conditioned to saline at different times of the day, but not in the group that was preexposed and conditioned at the same time of day. The results confirm a previous report that the time of day can modulate taste aversion learning independently of other environmental cues. It is proposed that the features and duration of the habituation training to the temporal contexts used may be critical for time-dependent latent inhibition to appear.     

Ethanol-mediated taste aversions and state-dependency in preweanling (16-day-old) rats

Requirements for conditioning of an ethanol-mediated taste aversion in 16-day-old rat pups were examined. Experiment 1 demonstrated that preweanling rats are capable of acquiring, in two trials, an aversion to a 15% sucrose solution when followed by intragastric intubation of a 1.2 g/kg dose of 17% v/v ethanol, but not when followed by a 0.4 g/kg dose. Comparison was with control animals given sucrose followed by an equivalent volume isocaloric Half and Half. When the 0.4 g/kg dose of ethanol preceded sucrose presentation by 30 min (Experiment 2), the aversion was learned, suggesting that the effective delay between the sucrose and the critical consequences of the ethanol had been too long with the former procedure. Expression of the sucrose aversion required, however, the reinstatement of the context of intoxication--state-dependent retention. Finally, the results of Experiment 3B indicated that, in addition to the association between the sucrose and the aversive consequences of alcohol intoxication, the orosensory cues resulting from alcohol's direct elimination, via such processes as respiration and salivation, became associated with the appetitive properties of the sucrose. This was evidenced by a conditioned increase in preference for ethanol odor. Possible age-related differences in the ability to associate stimuli with alcohol's unconditioned consequences, and in state dependency are discussed.     

Learned taste aversions in rats as a function of delay,speed, and duration of rotation

Rats fed a saccharin solution and then rotated on a turntable showed an aversion to the saccharin solution on later testing. In the first experiment, the rats learned to avoid saccharin with delays of as much as 9 hr between drinking the saccharin and the start of rotation. The second experiment showed that the critical determinant of aversiveness of rotation was number of rotations. The rats avoided saccharin as much after rotation at high speeds for short durations as after rotation at low speeds for long durations.     

Extinction of conditioned taste aversions: Effects of concentration and overshadowing

Extinction of conditioned taste aversions was examined as a function of taste concentration and of the presence of an additional taste. The results of Experiment 1 were consistent with previous evidence in that a conditioned aversion to high concentration saline was more persistent in extinction than an aversion to a low concentration. However, when floor effects were avoided the rate of extinction was faster for the higher (1%) concentration than for 0.2% saline (Experiment 2), a result consistent with accounts of extinction in other preparations. Three further experiments examined extinction of a conditioned sucrose aversion. The addition of 1% saline, but not of 0.2% saline, to sucrose during extinction produced overshadowing ("protection from extinction"; Experiment 3). Such overshadowing by saline was detected after two, but not after a single extinction trial (Experiment 4). This last finding suggests that under the conditions of the present experiments sweet and salty tastes function as elemental stimuli competing for loss of associative strength. No overshadowing was found when almond (an aqueous odour) was used in place of saline as the added stimulus, even when high concentrations of almond were used that produced observable neophobia (Experiments 5A and 5B).