Comparing neural response to painful electrical stimulation with functional MRI at 3 and 7T

Progressing from 3T to 7 T functional MRI enables marked improvements of human brain imaging in vivo. Although direct comparisons demonstrated advantages concerning blood oxygen level dependent (BOLD) signal response and spatial specificity, these mostly focused on single brain regions with rather simple tasks. Considering that physiological noise also increases with higher field strength, it is not entirely clear whether the advantages of 7T translate equally to the entire brain during tasks which elicit more complex neuronal processing. Therefore, we investigated the difference between 3T and 7 T in response to transcutaneous electrical painful and non-painful stimulation in 22 healthy subjects. For painful stimuli vs. baseline, stronger activations were observed at 7 T in several brain regions including the insula and supplementary motor area, but not the secondary somatosensory cortex (p<0.05 FWE-corrected). Contrasting painful vs. non-painful stimulation limited the differences between the field strengths to the periaqueductal gray (PAG, p<0.001 uncorrected) due to a similar signal increase at 7 T for both the target and specific control condition in most brain regions. This regional specificity obtained for the PAG at higher field strengths was confirmed by an additional spatial normalization strategy optimized for the brainstem. Here, robust BOLD responses were obtained in the dorsal PAG at 7 T (p<0.05 FWE-corrected), whereas at 3T activation was completely missing for the contrast against non-painful stimuli. To summarize, our findings support previously reported benefits obtained at ultra-high field strengths also for complex activation patterns elicited by painful electrical stimulation. However, this advantage depends on the region and even more on the contrast of interest. The greatest gain at 7 T was observed within the small brainstem region of the PAG, where the increased field strength offered marked improvement for the localization of activation foci with high spatial specificity.

[1]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[2]  Rao P. Gullapalli,et al.  The role of circulating sex hormones in menstrual cycle–dependent modulation of pain-related brain activation , 2013, PAIN.

[3]  G. Kranz,et al.  High-resolution functional MRI of the human amygdala at 7 T , 2013, European journal of radiology.

[4]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[5]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

[6]  A. Beitz,et al.  The distribution of brain-stem and spinal cord nuclei associated with different frequencies of electroacupuncture analgesia , 1993, Pain.

[7]  Oliver Speck,et al.  The impact of physiological noise correction on fMRI at 7 T , 2011, NeuroImage.

[8]  R. Dolan,et al.  Classical fear conditioning in functional neuroimaging , 2000, Current Opinion in Neurobiology.

[9]  Pia Baldinger,et al.  Increased Neural Habituation in the Amygdala and Orbitofrontal Cortex in Social Anxiety Disorder Revealed by fMRI , 2012, PloS one.

[10]  K. Uğurbil,et al.  Microvascular BOLD contribution at 4 and 7 T in the human brain: Gradient‐echo and spin‐echo fMRI with suppression of blood effects , 2003, Magnetic resonance in medicine.

[11]  Peter G. Morris,et al.  fMRI at 1.5, 3 and 7 T: Characterising BOLD signal changes , 2009, NeuroImage.

[12]  A. Shmuel,et al.  Imaging brain function in humans at 7 Tesla , 2001, Magnetic resonance in medicine.

[13]  David N. Kennedy,et al.  Automated Brainstem Co-registration (ABC) for MRI , 2006, NeuroImage.

[14]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[15]  Lawrence L. Wald,et al.  Comparison of physiological noise at 1.5 T, 3 T and 7 T and optimization of fMRI acquisition parameters , 2005, NeuroImage.

[16]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[17]  G. Kranz,et al.  Differential modulation of the default mode network via serotonin-1A receptors , 2012, Proceedings of the National Academy of Sciences.

[18]  Ralf Deichmann,et al.  fMRI of the brainstem using dual-echo EPI , 2011, NeuroImage.

[19]  Simon B. Eickhoff,et al.  Coordinate-based meta-analysis of experimentally induced and chronic persistent neuropathic pain , 2011, NeuroImage.

[20]  Emma G Duerden,et al.  Localization of pain‐related brain activation: A meta‐analysis of neuroimaging data , 2013, Human brain mapping.

[21]  Gabriele Lohmann,et al.  Parcellation of human amygdala in vivo using ultra high field structural MRI , 2011, NeuroImage.

[22]  B. G. Marsden,et al.  On the distribution of the , 1973 .

[23]  A. May,et al.  Within‐session sensitization and between‐session habituation: A robust physiological response to repetitive painful heat stimulation , 2012, European journal of pain.

[25]  A. May,et al.  Sensory and sympathetic correlates of heat pain sensitization and habituation in men and women , 2012, European journal of pain.

[26]  Randy L. Gollub,et al.  Exploring the brain in pain: Activations, deactivations and their relation , 2010, PAIN.

[27]  Robert Turner,et al.  Ultrahigh field systems and applications at 7 T and beyond: Progress, pitfalls, and potential , 2012, Magnetic resonance in medicine.

[28]  J. Duyn,et al.  EPI‐BOLD fMRI of human motor cortex at 1.5 T and 3.0 T: Sensitivity dependence on echo time and acquisition bandwidth , 2004, Journal of magnetic resonance imaging : JMRI.

[29]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[30]  David Borsook,et al.  Neuroimaging of the periaqueductal gray: State of the field , 2012, NeuroImage.

[31]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[32]  Israel Liberzon,et al.  Habituation of Rostral Anterior Cingulate Cortex to Repeated Emotionally Salient Pictures , 2003, Neuropsychopharmacology.

[33]  J. Walker,et al.  Pain modulation by release of the endogenous cannabinoid anandamide. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  C. Büchel,et al.  Activation of the Opioidergic Descending Pain Control System Underlies Placebo Analgesia , 2009, Neuron.

[35]  Ewald Moser,et al.  7‐T MR—from research to clinical applications? , 2012, NMR in biomedicine.

[36]  David G Norris,et al.  High field human imaging , 2003, Journal of magnetic resonance imaging : JMRI.

[37]  Karl J. Friston,et al.  Slice-timing effects and their correction in functional MRI , 2011, NeuroImage.