Pain anticipation recruits the mesolimbic system and differentially modulates subsequent recognition memory

TY - JOUR

T1 - Pain anticipation recruits the mesolimbic system and differentially modulates subsequent recognition memory

AU - Bauch, Eva M

AU - Rausch, Vanessa H

AU - Bunzeck, Nico

N1 - Copyright © 2014 Wiley Periodicals, Inc.

PY - 2014/9/1

Y1 - 2014/9/1

N2 - The ability to encode information into long-term memory is not a passive process but can be influenced by motivational factors. While the mesolimbic system has long been associated with reward-driven memory enhancement, the precise neurobiology of processing aversive events and their effects on declarative learning remain unclear. To address this issue, human subjects encoded a series of scene images, which was combined with cues predicting an aversive electric shock with different probabilities (0.2, 0.5, 0.8). Subsequently, recognition memory for the scenes was tested using a remember/know procedure. In a behavioral experiment, shock probability had linear effects on familiarity and inverted u-shaped effects on recollection. While the behavioral effect was absent in experiment 2 (fMRI), at the neural level encoding-related activity in the hippocampus mimicked the recollection specific quadratic effect, whereas activity in the anterior parahippocampal gyrus mirrored the familiarity specific linear relationship that was evident in experiment 1. Importantly, the probability of upcoming shocks was linearly coded in the substantia nigra / ventral tegmental area, and pain associated brain regions, such as the insula, responded to shock delivery. Our results demonstrate that anticipating primary aversive events recruits the human mesolimbic system and differentially modulates declarative memory functions via medial temporal lobe structures.

AB - The ability to encode information into long-term memory is not a passive process but can be influenced by motivational factors. While the mesolimbic system has long been associated with reward-driven memory enhancement, the precise neurobiology of processing aversive events and their effects on declarative learning remain unclear. To address this issue, human subjects encoded a series of scene images, which was combined with cues predicting an aversive electric shock with different probabilities (0.2, 0.5, 0.8). Subsequently, recognition memory for the scenes was tested using a remember/know procedure. In a behavioral experiment, shock probability had linear effects on familiarity and inverted u-shaped effects on recollection. While the behavioral effect was absent in experiment 2 (fMRI), at the neural level encoding-related activity in the hippocampus mimicked the recollection specific quadratic effect, whereas activity in the anterior parahippocampal gyrus mirrored the familiarity specific linear relationship that was evident in experiment 1. Importantly, the probability of upcoming shocks was linearly coded in the substantia nigra / ventral tegmental area, and pain associated brain regions, such as the insula, responded to shock delivery. Our results demonstrate that anticipating primary aversive events recruits the human mesolimbic system and differentially modulates declarative memory functions via medial temporal lobe structures.

KW - Adult

KW - Anticipation, Psychological

KW - Brain

KW - Brain Mapping

KW - Cues

KW - Electroshock

KW - Female

KW - Humans

KW - Linear Models

KW - Magnetic Resonance Imaging

KW - Male

KW - Mental Recall

KW - Neural Pathways

KW - Neuropsychological Tests

KW - Pain Perception

KW - Photic Stimulation

KW - Probability

KW - Recognition (Psychology)

KW - Visual Perception

KW - Young Adult

U2 - 10.1002/hbm.22497

DO - 10.1002/hbm.22497

M3 - SCORING: Journal article

C2 - 24692164

VL - 35

SP - 4594

EP - 4606

JO - HUM BRAIN MAPP

JF - HUM BRAIN MAPP

SN - 1065-9471

IS - 9

ER -