Measuring Pavlovian appetitive conditioning in humans with the postauricular reflex

Abstract

Despite its evolutionary and clinical significance, appetitive conditioning has been rarely investigated in humans. It has been proposed that this discrepancy might stem from the difficulty in finding suitable appetitive stimuli that elicit strong physiological responses. However, this might also be due to a possible lack of sensitivity of the psychophysiological measures commonly used to index human appetitive conditioning. Here, we investigated whether the postauricular reflex—a vestigial muscle microreflex that is potentiated by pleasant stimuli relative to neutral and unpleasant stimuli—may provide a valid psychophysiological indicator of appetitive conditioning in humans. To this end, we used a delay differential appetitive conditioning procedure, in which a neutral stimulus was contingently paired with a pleasant odor (CS+), while another neutral stimulus was not associated with any odor (CS−). We measured the postauricular reflex, the startle eyeblink reflex, and skin conductance response (SCR) as learning indices. Taken together, our results indicate that the postauricular reflex was potentiated in response to the CS+ compared with the CS−, whereas this potentiation extinguished when the pleasant odor was no longer delivered. In contrast, we found no evidence for startle eyeblink reflex attenuation in response to the CS+ relative to the CS−, and no effect of appetitive conditioning was observed on SCR. These findings suggest that the postauricular reflex is a sensitive measure of human appetitive conditioning and constitutes a valuable tool for further shedding light on the basic mechanisms underlying emotional learning in humans.

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, ).…”

“…Although there exists a certain overlap, primary and secondary rewards are processed in distinct neural systems (Sescousse, Caldú, Segura, & Dreher, ). Both primary and secondary appetitive reinforcers rarely result in physiological responses comparable to those evoked by reinforcers in aversive conditioning research (e.g., pain and noise), and the appetitive value of the US is difficult to standardize (Martin‐Soelch et al, ; Stussi et al, ). Furthermore, the physiological responses toward secondary reinforcers may be weaker compared to those elicited by primary reinforcers (Andreatta & Pauli, ; Ebrahimi et al, ).…”

“…Associated with this is the second challenge facing human appetitive conditioning research, namely, the lack of an established gold standard measurement to assess conditioned responding. A frequently implemented method to confirm successful conditioning are ratings, for example, CS valence (Andreatta & Pauli, ; Ebrahimi et al, , 2019; Klucken et al, , 2009, , ; Prévost et al, ), CS dichotomous preference (Bray & O'Doherty, ; Kahnt, Heinzle, Park, & Haynes, ; Metereau & Dreher, ; Prévost et al, ), US expectancy (van den Akker, Havermans, & Jansen, ), and contingency awareness (Bray & O'Doherty, ; Ebrahimi et al, , ; Klucken et al, , 2009, , ; Stussi et al, ; Tapia León et al, ). A shortcoming of ratings is that they only reflect the explicit component of learning and are prone to influences of social desirability when the learning task is simple.…”

“…Therefore, a thorough investigation of appetitive associative learning should incorporate both explicit and implicit conditioning indices. Unfortunately, due to the scarcity of multi‐methodological studies that compare implicit learning parameters, along with nonstandardized approaches of analysis, it is still unclear which measure is most suited in appetitive conditioning experiments (Stussi et al, ; Wardle et al, ).…”

“…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, ).…”