Perceptual learning to discriminate the intensity and spatial location of nociceptive stimuli

Mancini, Flavia; Dolgevica, Karina; Steckelmacher, James; Haggard, Patrick; Friston, Karl J.; Iannetti, Gian Domenico

doi:10.1038/srep39104

Cited by 14 publications

(13 citation statements)

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“…Finally, our findings inform a parallel debate about the localization of nociceptive cortex with a similar and longstanding discussion about the relative importance of somatosensory and insula cortices. There is sufficient evidence that nociceptive sensation involves fine-discriminative processing to imply cortical processing ( Mancini et al, 2012 ) and perceptual learning has been observed recently for nociceptive stimuli ( Mancini et al, 2016 ). It is even possible that there might be different loci for different submodalities of pain (heat, cold, mechanical, inflammatory pain, etc.).…”

Section: Discussionmentioning

confidence: 99%

Thermosensory Perceptual Learning Is Associated with Structural Brain Changes in Parietal–Opercular (SII) Cortex

et al. 2017

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The location of a sensory cortex for temperature perception remains a topic of substantial debate. Both the parietal–opercular (SII) and posterior insula have been consistently implicated in thermosensory processing, but neither region has yet been identified as the locus of fine temperature discrimination. Using a perceptual learning paradigm in male and female humans, we show improvement in discrimination accuracy for subdegree changes in both warmth and cool detection over 5 d of repetitive training. We found that increases in discriminative accuracy were specific to the temperature (cold or warm) being trained. Using structural imaging to look for plastic changes associated with perceptual learning, we identified symmetrical increases in gray matter volume in the SII cortex. Furthermore, we observed distinct, adjacent regions for cold and warm discrimination, with cold discrimination having a more anterior locus than warm. The results suggest that thermosensory discrimination is supported by functionally and anatomically distinct temperature-specific modules in the SII cortex.SIGNIFICANCE STATEMENT We provide behavioral and neuroanatomical evidence that perceptual learning is possible within the temperature system. We show that structural plasticity localizes to parietal–opercular (SII), and not posterior insula, providing the best evidence to date resolving a longstanding debate about the location of putative “temperature cortex.” Furthermore, we show that cold and warm pathways are behaviorally and anatomically dissociable, suggesting that the temperature system has distinct temperature-dependent processing modules.

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Section: Discussionmentioning

confidence: 99%

Thermosensory Perceptual Learning Is Associated with Structural Brain Changes in Parietal–Opercular (SII) Cortex

et al. 2017

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“…The laser device continuously samples the skin temperature at the stimulation site so that it can adjust its output energy to reach and maintain the target temperature. Importantly, this device can deliver stimuli lasting several seconds and is thus optimal for exploring the perceptual correlates of relatively slow increases and decreases in nociceptive input (Mancini et al 2016). The laser beam was transmitted through an optic fiber, and its diameter was set to 6 mm (28 mm 2 ) by focusing lenses.…”

Section: Methodsmentioning

confidence: 99%

No temporal contrast enhancement of simple decreases in noxious heat

Beck

Gnanasampanthan

Iannetti

et al. 2019

Journal of Neurophysiology

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Offset analgesia (OA) studies have found that small decreases in the intensity of a tonic noxious heat stimulus yield a disproportionately large amount of pain relief. In the classic OA paradigm, the decrease in stimulus intensity is preceded by an increase of equal size from an initial noxious level. Although the majority of researchers believe this temporal sequence of two changes is important for eliciting OA, it has also been suggested that the temporal contrast mechanism underlying OA may enhance detection of simple, isolated decreases in noxious heat. To test whether decreases in noxious heat intensity, by themselves, are perceived better than increases of comparable sizes, we used an adaptive two-interval alternative forced choice task to find perceptual thresholds for increases and decreases in radiant and contact heat. Decreases in noxious heat were more difficult to perceive than increases of comparable sizes from the same initial temperature of 45°C. In contrast, decreases and increases were perceived equally well within a common range of noxious temperatures (i.e., when increases started from 45°C and decreases started from 47°C). In another task, participants rated the pain intensity of heat stimuli that randomly and unpredictably increased, decreased, or remained constant. Ratings of unpredictable stimulus decreases also showed no evidence of perceptual enhancement. Our results demonstrate that there is no temporal contrast enhancement of simple, isolated decreases in noxious heat intensity. Combined with previous OA findings, they suggest that long-lasting noxious stimuli that follow an increase-decrease pattern may be important for eliciting the OA effect. NEW & NOTEWORTHY Previous research suggested that a small decrease in noxious heat intensity feels surprisingly large because of sensory enhancement of noxious stimulus offsets (a simplified form of “offset analgesia”). Using a two-alternative forced choice task where participants detected simple increases or decreases in noxious heat, we showed that decreases in noxious heat, by themselves, are no better perceived than increases of comparable sizes. This suggests that a decrease alone is not sufficient to elicit offset analgesia.

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“…Alternatively, other regions might have no role in the cause or expression of chronic pain, but instead reflect consequential (i.e. downstream) changes, for example perceptual learning of a new sensory environment in which pain is more common ( Mancini et al , 2016; Mano et al , 2017). Such regions might be expected to manifest later, and resolve with successful pain treatment ( Rodriguez-Raecke et al , 2009).…”

Section: Discussionmentioning

confidence: 99%

Classification and characterisation of brain network changes in chronic back pain: A multicenter study

Seymour¹,

Matsubara²,

Kotecha³

et al. 2018

Wellcome Open Res

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Background. Chronic pain is a common, often disabling condition thought to involve a combination of peripheral and central neurobiological factors. However, the extent and nature of changes in the brain is poorly understood. Methods. We investigated brain network architecture using resting-state fMRI data in chronic back pain patients in the UK and Japan (41 patients, 56 controls), as well as open data from USA. We applied machine learning and deep learning (conditional variational autoencoder architecture) methods to explore classification of patients/controls based on network connectivity. We then studied the network topology of the data, and developed a multislice modularity method to look for consensus evidence of modular reorganisation in chronic back pain. Results. Machine learning and deep learning allowed reliable classification of patients in a third, independent open data set with an accuracy of 63%, with 68% in cross validation of all data. We identified robust evidence of network hub disruption in chronic pain, most consistently with respect to clustering coefficient and betweenness centrality. We found a consensus pattern of modular reorganisation involving extensive, bilateral regions of sensorimotor cortex, and characterised primarily by negative reorganisation - a tendency for sensorimotor cortex nodes to be less inclined to form pairwise modular links with other brain nodes. In contrast, intraparietal sulcus displayed a propensity towards positive modular reorganisation, suggesting that it might have a role in forming modules associated with the chronic pain state. Conclusion. The results provide evidence of consistent and characteristic brain network changes in chronic pain, characterised primarily by extensive reorganisation of the network architecture of the sensorimotor cortex.

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Perceptual learning to discriminate the intensity and spatial location of nociceptive stimuli

Cited by 14 publications

References 50 publications

Thermosensory Perceptual Learning Is Associated with Structural Brain Changes in Parietal–Opercular (SII) Cortex

Thermosensory Perceptual Learning Is Associated with Structural Brain Changes in Parietal–Opercular (SII) Cortex

No temporal contrast enhancement of simple decreases in noxious heat

Classification and characterisation of brain network changes in chronic back pain: A multicenter study

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