Pain-specific modulation of hippocampal activity and functional connectivity during visual encoding

TY - JOUR

T1 - Pain-specific modulation of hippocampal activity and functional connectivity during visual encoding

AU - Forkmann, Katarina

AU - Wiech, Katja

AU - Ritter, Christoph

AU - Sommer-Blöchl, Tobias

AU - Rose, Michael

AU - Bingel, Ulrike

PY - 2013/2/6

Y1 - 2013/2/6

N2 - Acute and chronic pain automatically attract attention and thus interfere with cognitive functioning. Impaired memory is a prominent complaint of patients with chronic pain that substantially contributes to pain-related disability. In this fMRI study, we investigated the specific influence of pain on neural processes of memory encoding in healthy human volunteers using a visual task. To investigate the specificity of the interruptive effect of pain on the encoding of visual objects, objects were presented (1) alone, (2) with painful heat stimuli, or (3) with auditory stimuli that were matched for unpleasantness to the heat stimuli. The interruptive effect of concomitant aversive stimulation on behavioral measures and neural processing was assessed in a categorization task during encoding and in a subsequent recognition task. Pain interfered with object processing and encoding of visual stimuli. On the behavioral level, this resulted in slower reaction times during the categorization task for pain compared with auditory stimuli and in a lower recognition rate in the pain condition but not in the tone condition. Pain catastrophizing amplified this interruptive effect of pain. On the neural level, this pain-related disruption of encoding was associated with reduced activity in the right anterior hippocampus during encoding. Moreover, the hippocampus exhibited reduced functional connectivity with extrastriate regions during painful stimulation relative to auditory stimulation. In summary, our results show a pain-related disruption of visual encoding over and above the unpleasantness of a stimulus, suggesting a pain-specific interruptive mechanism that interferes with an early stage of memory formation.

AB - Acute and chronic pain automatically attract attention and thus interfere with cognitive functioning. Impaired memory is a prominent complaint of patients with chronic pain that substantially contributes to pain-related disability. In this fMRI study, we investigated the specific influence of pain on neural processes of memory encoding in healthy human volunteers using a visual task. To investigate the specificity of the interruptive effect of pain on the encoding of visual objects, objects were presented (1) alone, (2) with painful heat stimuli, or (3) with auditory stimuli that were matched for unpleasantness to the heat stimuli. The interruptive effect of concomitant aversive stimulation on behavioral measures and neural processing was assessed in a categorization task during encoding and in a subsequent recognition task. Pain interfered with object processing and encoding of visual stimuli. On the behavioral level, this resulted in slower reaction times during the categorization task for pain compared with auditory stimuli and in a lower recognition rate in the pain condition but not in the tone condition. Pain catastrophizing amplified this interruptive effect of pain. On the neural level, this pain-related disruption of encoding was associated with reduced activity in the right anterior hippocampus during encoding. Moreover, the hippocampus exhibited reduced functional connectivity with extrastriate regions during painful stimulation relative to auditory stimulation. In summary, our results show a pain-related disruption of visual encoding over and above the unpleasantness of a stimulus, suggesting a pain-specific interruptive mechanism that interferes with an early stage of memory formation.

KW - Acoustic Stimulation

KW - Adult

KW - Female

KW - Hippocampus

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Neural Pathways

KW - Pain

KW - Pain Measurement

KW - Pattern Recognition, Visual

KW - Photic Stimulation

KW - Psychomotor Performance

KW - Young Adult

U2 - 10.1523/JNEUROSCI.2994-12.2013

DO - 10.1523/JNEUROSCI.2994-12.2013

M3 - SCORING: Journal article

C2 - 23392685

VL - 33

SP - 2571

EP - 2581

JO - J NEUROSCI

JF - J NEUROSCI

SN - 0270-6474

IS - 6

ER -