From the neuromatrix to the pain matrix, and back (Iannetti and Mouraux)

From the neuromatrix to the pain matrix (and back)
G. D. Iannetti 1 and A. Mouraux2
(I actually met Iannetti at the IASP Congress held in Montreal this September 2010!)

(1) Department of Neuroscience, Physiology and Pharmacology, University College London, Medical Sciences Building, Gower Street, London, WC1E 6BT, UK
(2) Institute of Neurosciences (IONS), Université catholique de Louvain, Brussels, Belgium

G. D. Iannetti
Email: g.iannetti@ucl.ac.uk
Received: 4 January 2010 Accepted: 14 June 2010 Published online: 6 July 2010

Abstract
Pain is a conscious experience, crucial for survival. To investigate the neural basis of pain perception in humans, a large number of investigators apply noxious stimuli to the body of volunteers while sampling brain activity using different functional neuroimaging techniques. These responses have been shown to originate from an extensive network of brain regions, which has been christened the Pain Matrix and is often considered to represent a unique cerebral signature for pain perception. As a consequence, the Pain Matrix is often used to understand the neural mechanisms of pain in health and disease. Because the interpretation of a great number of experimental studies relies on the assumption that the brain responses elicited by nociceptive stimuli reflect the activity of a cortical network that is at least partially specific for pain, it appears crucial to ascertain whether this notion is supported by unequivocal experimental evidence. Here, we will review the original concept of the “Neuromatrix” as it was initially proposed by Melzack and its subsequent transformation into a pain-specific matrix. Through a critical discussion of the evidence in favor and against this concept of pain specificity, we show that the fraction of the neuronal activity measured using currently available macroscopic functional neuroimaging techniques (e.g., EEG, MEG, fMRI, PET) in response to transient nociceptive stimulation is likely to be largely unspecific for nociception.
Keywords Nociception – Pain matrix – Saliency – Multimodal – fMRI – EEG

Conclusion
We provide evidence suggesting that the brain responses to nociceptive stimuli measured using functional neuroimaging techniques that sample neural activity at population level (i.e., EEG, MEG, fMRI, PET) do not reflect nociceptive-specific brain activities, but, instead, brain activities equally involved in processing nociceptive and non-nociceptive salient sensory input. We hypothesize that at least part of these responses are involved in the detection of salient sensory events, regardless of whether these sensory events are conveyed by nociceptive pathways and also regardless of whether they are perceived as painful. Therefore, we suggest that the term “Pain Matrix” should be used with caution, because it misleadingly implies that the recorded responses are specific for pain.

Importantly, our hypothesis by no means implies the lack of assemblies of neurons whose activity is uniquely related to the perception of pain, or that the responses to nociceptive stimuli sampled by functional neuroimaging techniques do not reflect a crucial function for nociception. Instead, it suggests that these neuroimaging responses reflect a function that is crucial for all sensory systems: the ability to detect and react to salient (and possibly threatening) sensory input and thereby trigger swift and appropriate behavioral responses.

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