Control of appetitive and aversive taste-reactivity responses by an auditory conditioned stimulus in a devaluation task: A FOS and behavioral analysis

Abstract

Through associative learning, cues for biologically significant reinforcers such as food may gain access to mental representations of those reinforcers. Here, we used devaluation procedures, behavioral assessment of hedonic taste-reactivity responses, and measurement of immediate-early gene (IEG) expression to show that a cue for food engages behavior and brain activity related to sensory and hedonic processing of that food. Rats first received a tone paired with intraoral infusion of sucrose. Then, in the absence of the tone, the value of sucrose was reduced (Devalue group) by pairing sucrose with lithium chloride (LiCl), or maintained (Maintain group) by presenting sucrose and LiCl unpaired. Finally, taste-reactivity responses to the tone were assessed in the absence of sucrose. Devalue rats showed high levels of aversive responses and minimal appetitive responses, whereas Maintain rats exhibited substantial appetitive responding but little aversive responding. Control rats that had not received tone-sucrose pairings did not display either class of behaviors. Devalue rats showed greater FOS expression than Maintain rats in several brain regions implicated in devaluation task performance and the display of aversive responses, including the basolateral amygdala, orbitofrontal cortex, gustatory cortex (GC), and the posterior accumbens shell (ACBs), whereas the opposite pattern was found in the anterior ACBs. Both Devalue and Maintain rats showed greater FOS expression than control rats in amygdala central nucleus, GC, and both subregions of ACBs. Thus, through associative learning, auditory cues for food gained access to neural processing in several brain regions importantly involved in the processing of taste memory information.Reinforcer devaluation procedures are often used to assess cues' ability to guide behavior based on their access to a representation of the current incentive value of the reinforcer. For example, after tone-food pairings, the establishment of an aversion to the food reinforcer results in the spontaneous reduction of rats' learned food-cup approach responses to the tone, when it is presented later in the absence of food (Holland and Straub 1979). Thus, the rats' response to the tone is sensitive to changes in reinforcer value, despite no explicit experience of the tone together with the devalued reinforcer. Recent studies (for review, see Holland and Gallagher 2004) showed that this sensitivity of previously learned behaviors to subsequent alterations in reinforcer value demands function of a brain system that includes the basolateral amygdala (BLA) and the lateral orbitofrontal cortex (OFC).Previous devaluation studies examined changes in performance of learned responses preparatory to the receipt of food, such as food-cup approach. Here, we considered whether a learned cue for food would provoke consummatory responses that reflect the current sensory-hedonic aspects of food. In the absence of food itself, would a food cue provoke "liking" or "disgust" responses appropriate to the current...

Amount of training and cue-evoked taste-reactivity responding in reinforcer devaluation.

“…Furthermore, the performance of control rats that received the two CSs unpaired with the US indicated that the shift in response form we observed with extended training in the other groups did not reflect habituation of unconditioned positive responses to the auditory CSs or some other nonassociative factor. Our results also differed somewhat from those of Kerfoot et al (2007). First, here we found no evidence for the auditory CS's control over TR responses until after the unflavored water substrate was provided (CS + water or post-CS periods), whereas Kerfoot et al (2007) observed low but significant levels of such control during CS presentations even before presentation of the water substrate.…”

“…Our results also differed somewhat from those of Kerfoot et al (2007). First, here we found no evidence for the auditory CS's control over TR responses until after the unflavored water substrate was provided (CS + water or post-CS periods), whereas Kerfoot et al (2007) observed low but significant levels of such control during CS presentations even before presentation of the water substrate. Second, we found no evidence of spontaneous transfer of the aversive TR response established to sucrose itself during devaluation training in Group Devalue, to either auditory CS.…”

“…Second, we found no evidence of spontaneous transfer of the aversive TR response established to sucrose itself during devaluation training in Group Devalue, to either auditory CS. By contrast, Kerfoot et al (2007) found substantial display of aversive TRs to a CS after devaluation of its sucrose reinforcer.Notably, in Kerfoot et al's (2007) study, the sucrose US was presented intraorally throughout the experiment, whereas in Experiment 1, sucrose was delivered to a food cup, which required appetitive approach behaviors and generated somewhat different consummatory responses than are observed with intraoral fluid administration. Previous findings from other laboratories suggest that this procedural difference may have contributed to the differences in responding to the minimally-trained CS observed in Experiment 1 compared to Kerfoot et al's (2007) study.…”

“…Thus, there was no basis for S-R learning of negative TRs in Group Devalue. Finally, the control rats showed little evidence for TR responding.In the present study, we combined the methods of Holland (1998Holland ( , 2005 and Kerfoot et al (2007) to examine changes in the ability of auditory CSs paired with sucrose to activate evaluative processing of the sucrose. As in Holland's (2005) mediated taste aversion and devaluation studies, in each experiment, the rats first received 16 pairings of one auditory CS with sucrose ("minimal training") and 112 pairings of another CS with sucrose ("extensive training"), randomly intermixed within 8 sessions.…”

Disentangling pleasure from incentive salience and learning signals in brain reward circuitry

“…We assessed hedonic impact further by measuring orofacial reactions to the Pavlovian CS+ cues, which in principle, can acquire conditioned hedonic value as well as incentive value from their paired UCS (55)(56)(57)(58)(59)(60). The CS+1 tone occasionally and the CS+2 more frequently elicited a few positive hedonic reactions (on average, 1 reaction per 10 s under vehicle condition; this weak hedonic conditioned response was only 12% of the UCS unconditioned level of 8.3 per 10 s, but tone-elicited reactions were still mildly elevated over near-zero pre-CS baseline levels; CS+2: F 1,157 = 8.30, P < 0.01; CS+1: F 1,157 = 3.82, P = 0.052) (Fig.…”