The Human Centromedial Amygdala Contributes to Negative Prediction Error Signaling during Appetitive and Aversive Pavlovian Gustatory Learning.

Autor: Kolada E; Neurobiology of Emotions Laboratory, Centre of Excellence for Neural Plasticity and Brain Disorders (BrainCity), Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland e.kolada@nencki.edu.pl i.szatkowska@nencki.edu.pl., Bielski K; Neurobiology of Emotions Laboratory, Centre of Excellence for Neural Plasticity and Brain Disorders (BrainCity), Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland., Wilk M; Neurobiology of Emotions Laboratory, Centre of Excellence for Neural Plasticity and Brain Disorders (BrainCity), Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland., Rymarczyk K; Behavioral Neuroscience Laboratory, Department of Biological Psychology, SWPS University, 03-815 Warsaw, Poland., Bogorodzki P; Institute of Radioelectronics and Multimedia Technology, Warsaw University of Technology, 00-665 Warsaw, Poland., Kazulo P; Institute of Radioelectronics and Multimedia Technology, Warsaw University of Technology, 00-665 Warsaw, Poland., Kossowski B; Laboratory of Brain Imaging, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland., Wypych M; Laboratory of Brain Imaging, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland., Marchewka A; Laboratory of Brain Imaging, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland., Kaczmarek L; Laboratory of Neurobiology, Centre of Excellence for Neural Plasticity and Brain Disorders (BrainCity), Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, 02-093, Poland., Knapska E; Neurobiology of Emotions Laboratory, Centre of Excellence for Neural Plasticity and Brain Disorders (BrainCity), Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland., Szatkowska I; Neurobiology of Emotions Laboratory, Centre of Excellence for Neural Plasticity and Brain Disorders (BrainCity), Nencki Institute of Experimental Biology, Polish Academy of Sciences, 02-093 Warsaw, Poland e.kolada@nencki.edu.pl i.szatkowska@nencki.edu.pl.
Jazyk: angličtina
Zdroj: The Journal of neuroscience : the official journal of the Society for Neuroscience [J Neurosci] 2023 Apr 26; Vol. 43 (17), pp. 3176-3185. Date of Electronic Publication: 2023 Mar 24.
DOI: 10.1523/JNEUROSCI.0926-22.2023
Abstrakt: Prediction error (PE) is the mismatch between a prior expectation and reality, and it lies at the core of associative learning about aversive and appetitive stimuli. Human studies on fear learning have linked the amygdala to aversive PEs. In contrast, the relationship between the amygdala and PE in appetitive settings and stimuli, unlike those that induce fear, has received less research attention. Animal studies show that the amygdala is a functionally heterogeneous structure. Nevertheless, the role of the amygdala nuclei in PE signaling remains unknown in humans. To clarify the role of two subdivisions of the human amygdala, the centromedial amygdala (CMA) and basolateral amygdala (BLA), in appetitive and aversive PE signaling, we used gustatory pavlovian learning involving eating-related naturalistic outcomes. Thirty-eight right-handed individuals (19 females) participated in the study. We found that surprise with neutral feedback when a reward is expected triggers activity within the left and right CMA. When an aversive outcome is expected, surprise with neutral feedback triggers activity only within the left CMA. Notably, the BLA was not activated by those conditions. Thus, the CMA engages in negative PE signaling during appetitive and aversive gustatory pavlovian learning, whereas the BLA is not critical for this process. In addition, PE-related activity within the left CMA during aversive learning is negatively correlated with neuroticism and positively correlated with extraversion. The findings indicate the importance of the CMA in gustatory learning when the value of outcomes changes and have implications for understanding psychological conditions that manifest perturbed processing of negative PEs. SIGNIFICANCE STATEMENT A discrepancy between a prediction and an actual outcome (PE) plays a crucial role in learning. Learning improves when an outcome is more significant than expected (positive PE) and worsens when it is smaller than expected (negative PE). We found that the negative PE during appetitive and aversive taste learning is associated with increased activity of the CMA, which suggests that the CMA controls taste learning. Our findings may have implications for understanding psychological states associated with deficient learning from negative PEs, such as obesity and addictive behaviors.
(Copyright © 2023 Kolada et al.)
Databáze: MEDLINE