EPS Prize Lecture. Licking and liking: the assessment of hedonic responses in rodents

Affective processes are a key determinant of behaviour: At its simplest, liked stimuli are approached while disliked stimuli are avoided. Although assessing hedonic responses in nonverbal animals can be difficult, one relatively tractable approach relies on detailed analyses of rodents' consummatory behaviour. Rodents typically produce rhythmic sets of licks that can be grouped into clusters on the basis of the intervals between licks. The mean number of licks in a cluster (cluster size) is directly related to the concentration of palatable and unpalatable solutions. These relationships suggest that lick cluster size might be a useful index of an animal's hedonic reaction to the solution being consumed. I begin by reviewing studies of conditioned flavour preference and aversion that support the idea that lick cluster size can provide useful information about rats' hedonic reactions. I then describe how this methodology has been used to address previously intractable issues in the investigation of contrast effects as well as revealing an analogue of effort justification effects that, in humans, are commonly explained in terms of cognitive dissonance reduction. Finally, I consider how lick analysis might provide information about hedonic responses in animal models of human psychiatric disorders. In all these cases, how an animal did something was particularly informative about why it was doing it.     

Microstructural analysis of ingestive behaviour reveals no contribution of palatability to the incomplete extinction of a conditioned taste aversion

An analysis of the microstructure of licking responses was used to investigate the effects of conditioning and extinguishing a taste aversion. Rats received a single pairing of 8% fructose with lithium chloride (LiCl) while controls received unpaired exposure to fructose and LiCl. Pairing fructose with LiCl produced a reduction both in consumption and in the size of licking clusters. Subsequent exposure to fructose in the absence of LiCl produced some extinction of the taste aversion although at asymptote there was a residual difference in consumption between the taste aversion group and unpaired controls. In contrast the reduction in lick cluster size did completely extinguish. Previous analyses of licking microstructure indicate that lick cluster size is related to the palatability of the ingested solution. Thus these results indicate that although taste aversion learning initially reduces the palatability of the cue solution this reduction is not permanent. These results are discussed with reference to the possibility that preparatory behaviours are more resistant to extinction than are consummatory behaviours.     

Licking and liking: The assessment of hedonic responses in rodents

Affective processes are a key determinant of behaviour: At its simplest, liked stimuli are approached while disliked stimuli are avoided. Although assessing hedonic responses in nonverbal animals can be difficult, one relatively tractable approach relies on detailed analyses of rodents' consummatory behaviour. Rodents typically produce rhythmic sets of licks that can be grouped into clusters on the basis of the intervals between licks. The mean number of licks in a cluster (cluster size) is directly related to the concentration of palatable and unpalatable solutions. These relationships suggest that lick cluster size might be a useful index of an animal's hedonic reaction to the solution being consumed. I begin by reviewing studies of conditioned flavour preference and aversion that support the idea that lick cluster size can provide useful information about rats' hedonic reactions. I then describe how this methodology has been used to address previously intractable issues in the investigation of contrast effects as well as revealing an analogue of effort justification effects that, in humans, are commonly explained in terms of cognitive dissonance reduction. Finally, I consider how lick analysis might provide information about hedonic responses in animal models of human psychiatric disorders. In all these cases, how an animal did something was particularly informative about why it was doing it.

     

Consummatory Contrast Effects in Nondeprived Rats Following Shifts in Sucrose Concentration

Successive positive and negative contrast effects in consummatory behavior were investigated following shifts in sucrose concentrations in nondeprived subjects. Forty-four male albino rats were given daily 5-min access to either a 4%- or 32%-sucrose solution across a 14-day preshift period. Subjects in each group were then assigned to either a control or shifted condition. Shifted groups were upshifted (4–32%) or downshifted (32–4%) for a 10-day postshift period. Negative contrast was apparent in both lick rate and time spent at the drinking tube across the first 4 days of postshift. Positive contrast effects were not obtained, but rather a significant effect opposite to positive contrast occurred. The improbability of the ceiling effect explanation for the present results is discussed. Differences relative to deprivation state and the role of perceptual (taste) factors in contrast effects are also examined.

     

Within-subjects positive and negative contrast effects in rats.

Rats were given alternating 1-min. access periods to 2 tubes containing either 32% or 4% sucrose solutions for daily 6-min. test sessions. Lick rate for 32% was higher under comparison (32 vs. 4) than noncomparison (32 vs. 32) conditions; and lick rate for 4% was lower under comparison conditions (4 vs. 32) than under noncomparison conditions (4 vs. 4). All sucrose conditions were varied within subjects and both positive and negative contrast were obtained with a small n. In addition to lick rate, intake and latency measures also revealed contrast effects. Deprivation conditions altered latency but not lick rate measures of contrast. Reducing the test session to 3 min. (alternating 30-sec. access periods) did not greatly affect contrast. Additional experiments provided evidence for distinct within-days and between-days contrast effects, as well as a between-groups contrast effect.     

The effect of type of behavior on behavior change caused by type of upcoming food substance

Previous research suggests that rats will decrease their consumption of a low-valued substance if a high-valued one will soon be available (anticipatory contrast), but will increase their rate of operant responding for a low-valued substance if a high-valued one will soon be available (positive induction). The present experiments tested whether rats would increase their operant rate of licking or lever pressing for 1% liquid-sucrose reinforcement when 32% sucrose reinforcement was upcoming in the same session. Results indicated that upcoming 32% sucrose increased rates of lever pressing for 1% sucrose, but did not produce similar increases in rates of licking. In fact, upcoming 32% sucrose significantly reduced lick rates in Experiment 2. The present results suggest that the different changes in behavior may be linked to the specific response that the subjects must engage in to obtain the reward (i.e., licking vs. lever pressing), and not to the function of the behavior (i.e., consummatory vs. operant) or to how frequently the substances are available (i.e., continuously vs. intermittently).     

Contrast effects in flavour preference learning

In four experiments the role of contrast effects in producing learned flavour preferences was examined. The experiments showed that contrast effects are pervasive in flavour preference learning, producing results that are often paradoxical from a traditional reinforcement point of view. In Experiment 1, rats preferred a reinforced flavour over a nonreinforced flavour more if the reinforcer was 1% sucrose than if the reinforcer was 8% sucrose. Because the cue flavour was dissolved in 8% sucrose, this represents an anticipatory positive contrast effect. In Experiment 2, the relationship between cue and consequence was shown to be important in flavour preference learning, as expected if contrast effects are involved. In Experiment 3, rats preferred a flavour that was reinforced 4 times, and they preferred this flavour more than one reinforced 8 times, presumably because the greater the expectancy of the consequence, the greater the anticipatory negative contrast. In Experiment 4, rats consumed less of 0.15% saccharin if they received 32% sucrose randomly 90 min either before or after the 0.15% saccharin than if they received only 0.15% saccharin, a simultaneous negative contrast effect.     

Effects of sucrose concentration and goal units on runway behavior in the rat

Experiment 1 investigated the between-S and within-S effects of sucrose concentration (32 and 6%) and number of goal units (equal volumes of sucrose presented in single or multiple goal cups). The goal-unit variable had no effect on behavior under any of several test conditions employed. Within-S effects of sucrose concentration were approximately equal to between-S effects; no contrast effects were found. When 64 and 6% sucrose solutions were used as reinforcers in Experiment 2, a simultaneous, but not a successive, negative contrast effect was found. Results were discussed in terms of possible functional differences between the successive and simultaneous contrast paradigms and between sucrose solutions and solid food as reinforcers.     

Behavior of Maudsley reactive and nonreactive rats (Rattus norvegicus) in three consummatory contrast paradigms

Maudsley reactive (MR/Har) and nonreactive (MNRA/Har) rats (Rattus norvegicus) were tested in successive, simultaneous, and anticipatory contrast procedures. The MR/Har rats showed smaller successive negative contrast effects than the MNRA/Har rats when shifted from 32% to 4% sucrose, and the degree of contrast was smaller in animals of both strains than that typically obtained with unselected Sprague-Dawley derived rats. Chlordiazepoxide (4 and 8 mg/kg), which typically reduces contrast, did not influence degree of contrast in rats of either strain. Animals of both strains showed positive and negative contrast in the simultaneous contrast procedure, but degree of contrast in both cases was smaller in rats of the MR/Har strain. Animals of both strains also showed anticipatory contrast when a 0.15% saccharin solution preceded 32% sucrose in once-per-day pairings. In terms of latency to initiate licking, the MNRA/Har rats showed a contrast effect, but the MR/Har rats showed a "reinforcement" effect--shorter latency when saccharin preceded sucrose than when saccharin preceded saccharin. Open-field tests showed typical strain differences: The MNRA/Har rats ambulated more, reared more, defecated less, and showed less thigmotaxis than the MR/Har rats.     

Positron lifetime study of an Al-1.7at.% Mg-1.1at.% Cu alloy

The behaviour of vacancies during isothermal ageing following quenching of an Al-1.7at.% Mg-1.1at.% Cu alloy has been studied by positron annihilation lifetime spectroscopy. The positron lifetime parameters vary in parallel with the Vickers hardness of the alloy, suggesting simultaneous migration of vacancies and changes in the size and concentration of vacancies containing clusters and dislocation loops. The results also explain the long hardness plateau observed previously in ageing experiments carried out between 100 and 240°C in terms of a continuous growth of Mg-Cu-vacancy clusters during ageing. The vacancy concentration of the clusters increases gradually until the setting in of the cluster Guinier-Preston-Bagaryatsky zone transformation.     

A comparison of operant licking and lever pressing in the rat

Two groups of rats were trained on a signaled, free-operant, avoidance procedure to lick or to lever press in order to avoid shock while water-deprived or satiated and, in the case of licking, while ingesting deionized water, isotonic saline, or 10% sucrose. The most effective avoidance licking occurred while the rats were water-deprived and ingesting 10% sucrose. Water deprivation level had no effect on lever pressing for shock avoidance. Two other groups of rats were operantly conditioned to lick or to lever press for food pellets while waterdeprived or satiated and, in the case of licking, while ingesting deionized water or 10% sucrose. The most effective licking for food reinforcement occurred while the rats were water-deprived and ingesting 10% sucrose. Water deprivation level had no effect on lever pressing for food reinforcement. The data indicated that effective operant licking must be supported by factors related to water regulation and taste palatability.     

Apparent Incentive Contrast Effects in Autoshaping with Rats

The effects of shifts in reward quality and quantity on Pavlovian acquisition were studied in rats. In Experiment 1, animals preexposed to unsignaled food pellets, 10% sucrose solution, or home cage controls subsequently received autoshaping training (response-independent lever-pellet or lever-solution pairings, in three groups each). Unsignaled preexposure to sucrose solution facilitated autoshaping for pellets (relative to unshifted controls), whereas unsignaled preexposure to pellets retarded autoshaping for sucrose solution. In Experiment 2, unsignaled preexposure to 30% sucrose solution impaired acquisition reinforced by food pellets, relative to 2% solution. Using a choice procedure, Experiment 3 demonstrated that rats prefer pellets to either 2 or 10% sucrose solutions, but they prefer the 30% solution to the pellets. Experiment 4 demonstrated the facilitatory effect after an upward shift in reward magnitude rather than quality (from 1 to 12 pellets), but provided weaker evidence for retardation following a downward magnitude shift. Experiment 5 was similar to Experiment 4, except that animals received autoshaping training from the outset. No evidence of successive positive contrast was obtained, but there was a significant successive negative contrast effect. Moreover, extinction was faster after acquisition with 12 pellets rather than 1. These results suggest the presence of incentive contrast effects under Pavlovian training conditions.     

Human taste contrast and self-reported measures of anxiety.

Successive negative taste contrast in humans was demonstrated with a common taste stimulus, i.e., cherry-flavored Kool-Aid. A total of 31 male and female college-aged participants rated a 7% sucrose solution which was cherry-flavored as less sweet when it was preceded by a 28% rather than a 7% sucrose solution which was cherry-flavored. Because drugs such as the benzodiazepines affect taste contrast in rats and act as anxiolytics in humans, the present experiment also examined whether several self-reported measures of anxiety were related to taste contrast in humans. Neither scores on Taylor's Manifest Anxiety Survey nor those on the State-Trait Anxiety Inventory were related to "sweetness" ratings or contrast effects.     

Taste aversion after ingestion of lithium chloride: An associative analysis

In five experiments with rats we examined the aversion established by consumption of a solution of lithium chloride (LiCl). Experiment 1 showed that consumption of LiCl established an aversion to saline (NaCl). Experiment 2 showed that the size of the aversion was reduced in rats given pre-exposure to saline (a latent inhibition effect). Experiment 3 showed that experience of a sucrose-saline compound prior to consumption of LiCl generated an aversion to sucrose (a sensory preconditioning effect). Experiments 4 and 5 examined the effects produced by consumption of a sucrose-LiCl compound and demonstrated reciprocal overshadowing between the two tastes. These results confirm that consumption of LiCl establishes an aversion to the taste of this substance. Their implications for the use of orally consumed LiCl as a technique for the control of predatory behaviour are discussed.     

Reinforcer devaluation in palatability-based learned flavor preferences

Rats exposed to simultaneous compounds of 1 neutral flavor with dilute (2%) sucrose and a 2nd flavor with dilute (2%) maltodextrin subsequently consumed both flavors in preference to a 3rd flavor that was never paired with a palatable taste. Brief training exposure under ad lib food and water minimized the post-ingestive effects of nutrients, emphasizing the contribution of palatability to these preferences. Devaluation of sucrose or maltodextrin by pairing with illness (Experiment 1) or sensory-specific satiety (Experiment 2) selectively reduced the preference for the flavor previously paired with the devalued reinforcer. Such reinforcer-specific devaluation effects suggest that palatability-based learned flavor preferences are under-pinned by a Pavlovian process whereby the cue flavor is associated with the taste of the concurrently consumed palatable reinforcer.     

Induction when rats lick for 1% liquid-sucrose reinforcement

Previous research reported that rats responding for 1% liquid-sucrose reinforcement when 32% sucrose reinforcement is upcoming will decrease their response rate (contrast) if licking is the dependent measure and increase their response rate (induction) if pressing a lever is the dependent measure. The present study investigated whether induction could be observed when licking served as the dependent measure and whether induction in lever pressing and contrast in licking behaviour could be concurrently observed. Experiment 1 found induction when rats licked to earn the rewards but consumed them at a location separate from the spout licked to earn them. Experiment 2 also found induction when rats earned (and consumed) rewards by licking the same spout throughout the session. Experiment 3 separately measured instrumental lever pressing for sucrose rewards and licking the sucrose during the reward period. We found that both measures increased for 1% sucrose when 32% sucrose reinforcement was upcoming. The present results indicate that the type of response is not the sole determinant of whether contrast or induction is observed. Rather, they suggest that other procedural details, such as the location of reinforcer delivery, influence which effect is observed. The results also indicate that associative processes underlie the appearance of induction in responding for 1% sucrose.     

From contrast to reinforcement: role of response contingency in anticipatory contrast

Intake of a 0.15% saccharin solution is suppressed if access to the saccharin is followed by access to 32% sucrose in brief daily pairings. The present series of four experiments was concerned with factors that lead to this anticipatory contrast effect (suppressed saccharin intake) rather than a reinforcement effect. In Experiment 1, anticipatory contrast was obtained with an autoshaping procedure (no lick requirement on the initial tube), and degree of contrast did not vary as a function of intersolution interval in the range of 0-15 s. Experiments 2 and 3 showed that requirements of 10, 100, 200, or 400 licks on the first tube available led to a reinforcement effect in latency, but a requirement of 0 licks (autoshaping procedure) led to a contrast effect in licks and latency. In Experiment 4, a group with a 200-contingent-lick requirement showed a reinforcement effect in latency, but a group yoked to this contingent group showed a contrast effect in both latency and licks. Overall, the results suggest that anticipatory contrast occurs under conditions of a "relaxed" instrumental contingency. The data are discussed in terms of control of behavior by stimulus-stimulus, response-stimulus, and stimulus-response associations, and the results are related to behavioral contrast, to flavor-outcome associations, and to "misbehavior" produced by Pavlovian-instrumental interactions.     

Induction when rats lick for 1% liquid-sucrose reinforcement

Previous research reported that rats responding for 1% liquid-sucrose reinforcement when 32% sucrose reinforcement is upcoming will decrease their response rate (contrast) if licking is the dependent measure and increase their response rate (induction) if pressing a lever is the dependent measure. The present study investigated whether induction could be observed when licking served as the dependent measure and whether induction in lever pressing and contrast in licking behaviour could be concurrently observed. Experiment 1 found induction when rats licked to earn the rewards but consumed them at a location separate from the spout licked to earn them. Experiment 2 also found induction when rats earned (and consumed) rewards by licking the same spout throughout the session. Experiment 3 separately measured instrumental lever pressing for sucrose rewards and licking the sucrose during the reward period. We found that both measures increased for 1% sucrose when 32% sucrose reinforcement was upcoming. The present results indicate that the type of response is not the sole determinant of whether contrast or induction is observed. Rather, they suggest that other procedural details, such as the location of reinforcer delivery, influence which effect is observed. The results also indicate that associative processes underlie the appearance of induction in responding for 1% sucrose.     

Evidence for inhibitory associations between the unique elements of two compound flavours

In each of two experiments, rats were pre-exposed to two flavoured solutions, saline-lemon and sucrose-lemon. For group ALT, trials with one solution alternated with trials with the other. Group BLK received all trials with one solution in a block, before any trials with the other. An associative theory suggests that the alternating, but not the blocked, schedule would establish an inhibitory association between sucrose and saline. To provide a retardation test of this inhibition, some animals in each group were then given a single pairing of saline and sucrose, experienced sodium depletion, and were finally tested for their consumption of sucrose. Sodium depletion increased consumption of sucrose more in group BLK than in group ALT. In groups given no saline-sucrose pairing, sodium depletion had only a small effect on sucrose consumption, which was the same in both groups. After multiple pairings of saline and sucrose, sodium depletion had an equally large effect on sucrose consumption in both ALT and BLK groups. These results imply that alternating pre-exposure to two compound solutions does establish an inhibitory association between their unique elements, and thus provide support for an associative theory of perceptual learning.     

Can contextual cues control consummatory successive negative contrast?

Rats exposed to incentive downshift show behavioral deterioration. This phenomenon, called successive negative contrast (SNC), occurs in instrumental and consummatory responses (iSNC, cSNC). Whereas iSNC is related to the violation of reward expectancies retrieved in anticipation of the goal (cued-recall), cSNC involves reward rejection and may require only recognition memory retrieved at consumption. The three within-subject experiments reported here suggest that cued-recall memory can also operate in cSNC under some conditions. A small but significant cSNC effect was obtained when animals were exposed to the conditioning context during an average 90-s interval before the introduction of the incentive (either 16% or 2% sucrose solutions), rather than being given immediate access to the sucrose upon entry into the context (Experiment 1). Neither simultaneous contrast (Experiment 2) nor simple sequential effects (Experiment 3) contribute to this within-subject version of cSNC. These results suggest that cSNC can be shifted to a cued-recall mode with appropriate training parameters.