Pupil dilation as an index of Pavlovian conditioning. A systematic review and meta-analysis

Finke, Johannes B.; Roesmann, Kati; Stalder, Tobias; Klucken, Tim

doi:10.1016/j.neubiorev.2021.09.005

Cited by 27 publications

(43 citation statements)

References 84 publications

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“…In studies 2 and 3 ( n = 79), pupil dilation responses were collected as an independent measure of anticipatory autonomic arousal ( Finke et al, 2021 ). Pupil size was recorded continuously throughout MRI scanning, using a remote nonferromagnetic infrared long range mount eye tracker (model EyeLink 1000, SR Research).…”

Section: Methodsmentioning

confidence: 99%

Robust BOLD Responses to Faces But Not to Conditioned Threat: Challenging the Amygdala's Reputation in Human Fear and Extinction Learning

et al. 2021

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Most of our knowledge about human emotional memory comes from animal research. Based on this work, the amygdala is often labeled the brain's “fear center”, but it is unclear to what degree neural circuitries underlying fear and extinction learning are conserved across species. Neuroimaging studies in humans yield conflicting findings, with many studies failing to show amygdala activation in response to learned threat. Such null findings are often treated as resulting from MRI-specific problems related to measuring deep brain structures. Here we test this assumption in a mega-analysis of three studies on fear acquisition ( n = 98; 68 female) and extinction learning ( n = 79; 53 female). The conditioning procedure involved the presentation of two pictures of faces and two pictures of houses: one of each pair was followed by an electric shock [a conditioned stimulus (CS + )], the other one was never followed by a shock (CS – ), and participants were instructed to learn these contingencies. Results revealed widespread responses to the CS + compared with the CS – in the fear network, including anterior insula, midcingulate cortex, thalamus, and bed nucleus of the stria terminalis, but not the amygdala, which actually responded stronger to the CS – . Results were independent of spatial smoothing, and of individual differences in trait anxiety and conditioned pupil responses. In contrast, robust amygdala activation distinguished faces from houses, refuting the idea that a poor signal could account for the absence of effects. Moving forward, we suggest that, apart from imaging larger samples at higher resolution, alternative statistical approaches may be used to identify cross-species similarities in fear and extinction learning. SIGNIFICANCE STATEMENT The science of emotional memory provides the foundation of numerous theories on psychopathology, including stress and anxiety disorders. This field relies heavily on animal research, which suggests a central role of the amygdala in fear learning and memory. However, this finding is not strongly corroborated by neuroimaging evidence in humans, and null findings are too easily explained away by methodological limitations inherent to imaging deep brain structures. In a large nonclinical sample, we find widespread BOLD activation in response to learned fear, but not in the amygdala. A poor signal could not account for the absence of effects. While these findings do not disprove the involvement of the amygdala in human fear learning, they challenge its typical portrayals and illustrate the complexities of translational science.

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Section: Methodsmentioning

confidence: 99%

Robust BOLD Responses to Faces But Not to Conditioned Threat: Challenging the Amygdala's Reputation in Human Fear and Extinction Learning

et al. 2021

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“…We found an interaction, starting from about 800 ms and sustained up to 2850 ms, in which, on average, smokers pupils tended to constrict more than non-smokers ones. This is interesting, albeit not entirely expected on the basis of evidence pointing to a robust role of pupil dilation in both appetitive and aversive conditioning (Finke et al, 2021). Moreover, the only previous study that assessed pupil size in response to NRS (Chae et al, 2008) reported pupil dilation in a sample of 7 smokers (against 12 controls), similarly to when viewing highly arousing images (regardless of their valence).…”

Section: Discussionmentioning

confidence: 79%

“…Pupil dilation reflects, beyond that, the activation of the autonomic system, and as such it ideally probes: affective and emotional responses to visual stimuli (Bogdanova et al, 2022; Dureux et al, 2021); the amount of cognitive effort deployed for a task (e.g., working memory load, Lisi et al, 2015; Mathôt, 2018); and, perhaps in light of the strict dialogue between the locus coeruleus and limbic areas subserving motivation, the subjective value of a given stimulus (Muhammed et al, 2016; Pietrock et al, 2019). Accordingly, a recent meta-analysis concluded that pupil dilation is a robust marker of Pavlovian-like conditioning (Finke et al, 2021). Despite these premises, however, studies attempting to characterize attentional capture by means of pupillometry are still scarce (but see Chae et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Pupil size as a robust marker of attentional bias toward nicotine-related stimuli in smokers

Blini

Zorzi

2022

Preprint

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Spatial attention can be magnetically attracted by behaviorally salient stimuli. This phenomenon occasionally conflicts with behavioral goals, leading to maladaptive consequences, as in the case of addiction, in which attentional biases have been described and linked with clinically meaningful variables, such as craving level or dependence intensity. Here, we sought to probe the markers of attentional priority in smokers through eye-tracking measures, by leveraging the established link between eye movements and spatial attention. We were particularly interested in potential markers related to pupil size, because pupil diameter reflects a range of autonomic, affective, and cognitive/attentional reactions to behaviorally significant stimuli and is a robust marker of appetitive and aversive learning. We found that changes in pupil size to nicotine-related visual stimuli could reliably predict, in crossvalidated logistic regression, the smoking status of young smokers (showing pupil constriction) better than more traditional proxy measures. The possibility that pupil constriction may reflect a bias toward central vision, e.g. attentional capture, is discussed in terms of sensory tuning with respect to nicotine-related stimuli. Pupil size was more sensitive at lower nicotine dependence levels, and at increased abstinence time (though these two variables were collinear). We conclude that pupillometry can provide a robust marker for attentional priority computation and useful indications regarding motivational states and individual attitudes toward conditioned stimuli.

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“…There is a nearly hundred-year background of studies of pupillary conditioning, including classical conditioning of autonomic responses, reported by Pavlov and Anrep (1927). In general, conditioning pupil dilation to unconditioned sensory stimuli, including sounds, touch, and pain, has been successful in both animals (most often cats) and humans (Finke et al, 2021), including infants (Brackbill & Fitzgerald, 1972). In contrast, attempts to classically condition the light reflex-that is, using a neutral stimulus to elicit a light-induced constriction-have failed to provide evidence of a conditioned light reaction, as Loewenfeld (1958) documented.…”

Section: Conditioningmentioning

confidence: 99%

Publication guidelines and recommendations for pupillary measurement in psychophysiological studies

et al. 2022

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A variety of psychological and physical phenomena elicit variations in the diameter of pupil of the eye. Changes in pupil size are mediated by the relative activation of the sphincter pupillae muscle (decrease pupil diameter) and the dilator pupillae muscle (increase pupil diameter), innervated by the parasympathetic and sympathetic branches, respectively, of the autonomic nervous system. The current guidelines are intended to inform and guide psychophysiological research involving pupil measurement by (1) summarizing important aspects concerning the physiology of the pupil, (2) providing methodological and data‐analytic guidelines and recommendations, and (3) briefly reviewing psychological phenomena that modulate pupillary reactivity. Because of the increased ease and tractability of pupil measurement, the goal of these guidelines is to promote accurate recording, analysis, and reporting of pupillary data in psychophysiological research.

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Pupil dilation as an index of Pavlovian conditioning. A systematic review and meta-analysis

Cited by 27 publications

References 84 publications

Robust BOLD Responses to Faces But Not to Conditioned Threat: Challenging the Amygdala's Reputation in Human Fear and Extinction Learning

Robust BOLD Responses to Faces But Not to Conditioned Threat: Challenging the Amygdala's Reputation in Human Fear and Extinction Learning

Pupil size as a robust marker of attentional bias toward nicotine-related stimuli in smokers

Publication guidelines and recommendations for pupillary measurement in psychophysiological studies

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