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ARTICLE, Behavioral/Systems

Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network

Alexander Ploghaus, Charvy Narain, Christian F. Beckmann, Stuart Clare, Susanna Bantick, Richard Wise, Paul M. Matthews, J. Nicholas P. Rawlins and Irene Tracey
Journal of Neuroscience 15 December 2001, 21 (24) 9896-9903; DOI: https://doi.org/10.1523/JNEUROSCI.21-24-09896.2001
Alexander Ploghaus
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
2Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom
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Charvy Narain
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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Christian F. Beckmann
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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Stuart Clare
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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Susanna Bantick
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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Richard Wise
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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Paul M. Matthews
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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J. Nicholas P. Rawlins
2Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom
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Irene Tracey
1Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, and
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  • Fig. 1.
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    Fig. 1.

    Relevant experimental conditions. Visual signals predicted painful heat stimulation to the back of the left hand. Painful stimulation was delivered either at a lower (LT) or at a discriminably higher (HT) temperature. One visual signal (here:triangle) was consistently followed by LT and came to evoke low anxiety (LA). Another signal (here:square) was followed by LT on most of the trials, but occasionally by HT, and came to evoke higher anxiety (HA). We studied anxiety-induced increases in perceived pain intensity by comparing brain responses to pain in conditions LT/HA and LT/LA. We also assessed temperature-induced increases in perceived pain intensity by comparing brain responses to pain in conditions HT/HA and LT/HA.

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    Fig. 2.

    Behavioral results. A, Ratings of anxiety during presentation of signals HA and LA before the onset of pain LT (bench control group, mean ± one SEM). B, Heart rate changes during presentation of signals HA and LA (scanner group, mean ± one SEM). C, Ratings of perceived pain intensity in conditions LT/LA, LT/HA, and HT/HA (scanner group, mean ± one SEM).

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    Fig. 3.

    Group Z value maps thresholded atp < 0.001 and superimposed on an average anatomical MRI of participating subjects in Talairach space (radiological convention). A, Significant activations associated with temperature-related increases in perceived pain (HT/HA vs LT/HA). The coronal view (left, y= −16) shows activations bilaterally in primary somatosensory cortex (SI), dorsal margin of the posterior insula (pI), thalamus, midcingulate cortex, and in the right hippocampus. The horizontal view (right,z = −14) depicts bilateral hippocampus as well as orbitofrontal cortex. B, Anxiety-related increases in perceived pain (LT/HA vs LT/LA) are associated with significant activation in the left entorhinal cortex. The activation area is shown in coronal (left, y = −16) and horizontal (right, z = −26) view.C, Areas showing activity significantly correlated with the entorhinal FMRI signal during pain modulation by anxiety (LT/HA and LT/LA). The coronal view (left, y = 36) and the horizontal view (right,z = 6) show activation in the perigenual cingulate cortex, and the horizontal view depicts bilateral activity in the mid-insular and parainsular cortices.

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    Fig. 4.

    Significantly different hemodynamic responses in the hippocampus proper and entorhinal cortex (group mean ± one SEM). Regional time courses of FMRI signal represent percentage of change from the rest period preceding each trial, averaged across trials and subjects. The period of painful stimulation is shaded.A, The hippocampus proper was significantly activated bilaterally during HT/HA (●) relative to LT/HA (▴).B, The left entorhinal cortex was significantly activated during LT/HA (▴) relative to LT/LA (▪), as well as relative to baseline. The right entorhinal cortex shows similar, but smaller responses, which is consistent with observations of left-lateralized processing of explicit aversive conditioning in the medial temporal lobes.

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    Table 1.

    Areas activated during exacerbation of pain by increases in anxiety or temperature

    Brain region (Brodmann area)SideTalairach coordinatesZvalueZ threshold
    XYZMeanMax.p= 0.05, cor.
    Pain modulation by anxiety
     Entorhinal cortex (28)L−22−17−263.574.613.44
     Mid-insula/parainsular cortex (52)*R44−1033.764.983.41
    L−53−1153.905.963.41
     Perigenual cingulate (24/32)*L/R13793.885.963.41
    Pain modulation by temperature
     HippocampusL−18−24−133.464.303.34
    R21−21−143.784.823.34
     Orbitofrontal cortex (11)L/R−158−133.464.333.34
     SI/MIL−52−13413.484.263.34
    R42−14483.775.813.34
     Posterior insulaL−39−19153.564.393.34
    R37−19143.604.633.34
     ThalamusL/R−1−923.754.903.34
     Midcingulate (24′/32′)L/R1−11464.026.203.34
    • p = 0.001; Z = 3.09.

    • ↵* Area shows activity significantly correlated with the entorhinal FMRI signal during LT/HA and LT/LA (p< 0.001).

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The Journal of Neuroscience: 21 (24)
Journal of Neuroscience
Vol. 21, Issue 24
15 Dec 2001
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Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network
Alexander Ploghaus, Charvy Narain, Christian F. Beckmann, Stuart Clare, Susanna Bantick, Richard Wise, Paul M. Matthews, J. Nicholas P. Rawlins, Irene Tracey
Journal of Neuroscience 15 December 2001, 21 (24) 9896-9903; DOI: 10.1523/JNEUROSCI.21-24-09896.2001

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Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network
Alexander Ploghaus, Charvy Narain, Christian F. Beckmann, Stuart Clare, Susanna Bantick, Richard Wise, Paul M. Matthews, J. Nicholas P. Rawlins, Irene Tracey
Journal of Neuroscience 15 December 2001, 21 (24) 9896-9903; DOI: 10.1523/JNEUROSCI.21-24-09896.2001
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Keywords

  • hyperalgesia
  • hippocampus
  • classical fear conditioning
  • anterior cingulate
  • insula
  • causal associative learning
  • medial temporal lobe
  • surprise
  • aversive emotional learning
  • anticipation
  • functional neuroimaging

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