Neural correlates of subjective CS/UCS association in appetitive conditioning

Abstract

Explicit knowledge of conditioned stimulus (CS)/unconditioned stimulus (UCS) associations is proposed as important factor in classical conditioning. However, while previous studies have focused on its roles in fear conditioning, it has been neglected in the context of appetitive conditioning. The present functional magnetic resonance study aimed to investigate neural activation and functional connectivity linked to subjective CS/UCS association in appetitive conditioning. In total, 85 subjects participated in an appetitive acquisition procedure in which a neutral stimulus (CS+) was paired with a monetary reward, while another neutral stimulus (CS-) was never paired with the reward. Directly afterwards, subjective CS/UCS association was assessed by measuring the extent to which the CS+ was thought to be associated with the UCS compared to the CS-. Close relationships were established between subjective CS/UCS association and activations in the primary visual cortex (V1) during the early phase of conditioning and in the striatum during the late conditioning phase. In addition, we observed inverse relationships between subjective CS/UCS association and both V1/ventromedial prefrontal cortex (vmPFC) and striatal/vmPFC connectivity. The results suggest the involvement of decoupling vmPFC connectivity in reward learning in general and the roles of attentional processes in the formation of the subjective CS/UCS association during the early phase and reward prediction during the late phase of appetitive conditioning.

Pupil dilation as an implicit measure of appetitive Pavlovian learning

“…Regarding the first, it is difficult to determine a US whose rewarding properties or subjective pleasantness is inter‐individually equivalent. So far, a variety of both primary and secondary stimuli have been used for appetitive reinforcement, for example, food (Andreatta & Pauli, ; Blechert, Testa, Georgii, Klimesch, & Wilhelm, ; van den Akker et al, ; Wardle, Lopez‐Gamundi, & Flagel, ), drink (Ebrahimi et al, ; O'Doherty, Buchanan, Seymour, & Dolan, ; O'Doherty, Dayan, Friston, Critchley, & Dolan, ; Pauli et al, ; Prévost, McNamee, Jessup, Bossaerts, & O’Doherty, ), odor (Gottfried, O'Doherty, & Dolan, ; Hermann, Ziegler, Birbaumer, & Flor, ; Stussi, Delplanque, Corai, Pourtois, & Sander, ), attractive faces (Bray & O'Doherty, ), erotic images (Klucken et al, , , ; Klucken, Wehrum‐Osinsky, Schweckendiek, Kruse, & Stark, ), and money (Austin & Duka, ; Delgado, Gillis, & Phelps, ; Ebrahimi et al, ; Tapia León, Kruse, Stalder, Stark, & Klucken, ). Although there exists a certain overlap, primary and secondary rewards are processed in distinct neural systems (Sescousse, Caldú, Segura, & Dreher, ).…”

“…Psychophysiological measures similarly often present inconsistent results. Electrodermal activity, which is a common learning index used in aversive conditioning paradigms (Lonsdorf et al, ; Ney et al, ), has shown both an enhanced skin conductance response (SCR; Andreatta & Pauli, ; Ebrahimi et al, ; Klucken et al, , , ; Tapia León et al, ), as well as no differential response (Klucken et al, ; Stussi et al, ; van den Akker et al, ) to the reward‐associated stimulus and appears to be dependent on task context (van den Akker et al, ). Heart period response (HPR) has seldom been examined in an appetitive context and has not yielded a conclusive differential effect (Hermann, Ziegler, Birbaumer, & Flor, ; Wardle et al, ).…”

Amygdala and nucleus accumbens involvement in appetitive extinction

“…In line with our findings, Chase et al () showed in their meta‐analysis that involvement of the amygdala is specific to acquisition of classical conditioning in contrast to tasks focusing instrumental learning. The NAcc has mainly been associated with acquiring the subjective CS/UCS‐association and contingency awareness (Klucken, Schweckendiek et al, ; Tapia León et al, ).…”

“…After few pairings, presenting the CS+ elicits conditioned responses as compared to the CS−. These include higher subjective ratings of valence and arousal, increased skin conductance responses (SCRs), and increased BOLD responses in brain areas associated with conditioning and reward processing (Andreatta & Pauli, ; Tapia León, Kruse, Stalder, Stark, & Klucken, ).…”

“…Brain regions associated with appetitive conditioning mainly include the amygdala, nucleus accumbens (NAcc), dorsal and ventral anterior cingulate cortex (dACC/vACC), orbitofrontal cortex (OFC), and caudate nucleus (Chase, Kumar, Eickhoff, & Dombrovski, ; Klucken, Tabbert et al, ; Klucken, Wehrum et al, ; Martin‐Soelch, Linthicum, & Ernst, ). In the context of acquisition of appetitive conditioning, the amygdala is thought to encode the association of the CS with the unconditioned reaction, whereas the NAcc has been associated with subjective CS/UCS‐association and the reward prediction error (O'Doherty, Dayan, Friston, Critchley, & Dolan, ; Tapia León et al, ). Within the anterior cingulate cortex, the vACC is thought to mediate early discriminatory learning in contrast to the dACC, which is thought to encode outcome expectancy (Alexander & Brown, ).…”