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.

Figure 1.

Mean ± SEM taste-reactivity responses in the test session. Each trial comprised a 10-sec pre-tone period, 10 sec of tone alone, 5 sec of tone accompanied by deionized water, and a 10 sec post-tone interval. Rats in group Maintain had received tone → sucrose pairings followed by sucrose and toxin unpaired. Rats in group Devalue had received tone → sucrose pairings followed by sucrose–toxin pairings. Rats in the two control (CTL) groups had received tone and sucrose unpaired followed by sucrose either paired (d, devalue) or unpaired (m, maintain) with toxin. (A) Appetitive responses; (B) aversive responses.

Figure 2.

Mean ± SEM FOS-immunoreactive cells/mm² in (A) basolateral amygdala (BLA), orbitofrontal cortex (OFC), gustatory cortex (GC) and (B) nucleus accumbens shell. Starred brackets indicate significant (P < 0.05) differences.