Contingency learning in human fear conditioning involves the ventral striatum

• Published in: Human brain mapping Vol. 30; no. 11; pp. 3636 - 3644
• Main Authors: Klucken, Tim, Tabbert, Katharina, Schweckendiek, Jan, Merz, Christian Josef, Kagerer, Sabine, Vaitl, Dieter, Stark, Rudolf
• Format: Journal Article
• Language: English
• Published: Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.11.2009; Wiley-Liss
• Subjects: Adult; Awareness - physiology; Basal Ganglia - blood supply; Basal Ganglia - drug effects; Basal Ganglia - physiology; Biological and medical sciences; Brain Mapping; Conditioning, Classical - drug effects; Conditioning, Classical - physiology; contingency awareness; Databases, Factual - statistics & numerical data; differential classical conditioning; Fear - drug effects; fear conditioning; Female; Fundamental and applied biological sciences. Psychology; Human; Humans; Hydrocortisone - pharmacology; Investigative techniques, diagnostic techniques (general aspects); Learning; Learning. Memory; Magnetic Resonance Imaging - methods; Male; Medical sciences; Models, Statistical; Nervous system; nucleus accumbens; Oxygen - blood; Psychology. Psychoanalysis. Psychiatry; Psychology. Psychophysiology; Radiodiagnosis. Nmr imagery. Nmr spectrometry; striatum; Young Adult; Human; Nervous system diseases; fear conditioning; Radiodiagnosis; Awareness; Central nervous system; contingency awareness; Basal ganglion; Corpus striatum; Encephalon; Learning; Nucleus accumbens; Fear; Acquisition process; striatum; differential classical conditioning; Conditioning
• ISSN: 1065-9471; 1097-0193; 1097-0193
• DOI: 10.1002/hbm.20791

The ability to detect and learn contingencies between fearful stimuli and their predictive cues is an important capacity to cope with the environment. Contingency awareness refers to the ability to verbalize the relationships between conditioned and unconditioned stimuli. Although there is a heated debate about the influence of contingency awareness on conditioned fear responses, neural correlates behind the formation process of contingency awareness have gained only little attention in human fear conditioning. Recent animal studies indicate that the ventral striatum (VS) could be involved in this process, but in human studies the VS is mostly associated with positive emotions. To examine this question, we reanalyzed four recently published classical fear conditioning studies (n = 117) with respect to the VS at three distinct levels of contingency awareness: subjects, who did not learn the contingencies (unaware), subjects, who learned the contingencies during the experiment (learned aware) and subjects, who were informed about the contingencies in advance (instructed aware). The results showed significantly increased activations in the left and right VS in learned aware compared to unaware subjects. Interestingly, this activation pattern was only found in learned but not in instructed aware subjects. We assume that the VS is not involved when contingency awareness does not develop during conditioning or when contingency awareness is unambiguously induced already prior to conditioning. VS involvement seems to be important for the transition from a contingency unaware to a contingency aware state. Implications for fear conditioning models as well as for the contingency awareness debate are discussed. Hum Brain Mapp, 2009. © 2009 Wiley‐Liss, Inc.