Expectation violation and attention to pain jointly modulate neural gain in somatosensory cortex

Francesca Fardo,Ryszard Auksztulewicz,Micah Allen,Martin J Dietz,Andreas Roepstorff,Karl J Friston

doi:10.1016/j.neuroimage.2017.03.041

Francesca Fardo, Ryszard Auksztulewicz + Show 4 more

Open Access

https://doi.org/10.1016/j.neuroimage.2017.03.041

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Abstract

The neural processing and experience of pain are influenced by both expectations and attention. For example, the amplitude of event-related pain responses is enhanced by both novel and unexpected pain, and by moving the focus of attention towards a painful stimulus. Under predictive coding, this congruence can be explained by appeal to a precision-weighting mechanism, which mediates bottom-up and top-down attentional processes by modulating the influence of feedforward and feedback signals throughout the cortical hierarchy. The influence of expectation and attention on pain processing can be mapped onto changes in effective connectivity between or within specific neuronal populations, using a canonical microcircuit (CMC) model of hierarchical processing. We thus implemented a CMC within dynamic causal modelling for magnetoencephalography in human subjects, to investigate how expectation violation and attention to pain modulate intrinsic (within-source) and extrinsic (between-source) connectivity in the somatosensory hierarchy. This enabled us to establish whether both expectancy and attentional processes are mediated by a similar precision-encoding mechanism within a network of somatosensory, frontal and parietal sources. We found that both unexpected and attended pain modulated the gain of superficial pyramidal cells in primary and secondary somatosensory cortex. This modulation occurred in the context of increased lateralized recurrent connectivity between somatosensory and fronto-parietal sources, driven by unexpected painful occurrences. Finally, the strength of effective connectivity parameters in S1, S2 and IFG predicted individual differences in subjective pain modulation ratings. Our findings suggest that neuromodulatory gain control in the somatosensory hierarchy underlies the influence of both expectation violation and attention on cortical processing and pain perception.

Highlights

Expectation and attention both exert a strong influence on pain perception (e.g., Wiech et al, 2008) and the magnitude of pain-related neural responses (e.g., Dowman, 2007; Legrain et al, 2009b)
In a group-level 2×2×2 repeated measures ANOVA, we modeled the experimental conditions (8 levels; unattended left standard (uLS), unattended left deviant (uLD), unattended right standard (uRS), unattended right deviant (uRD), attended left standard (aLS), attended left deviant (aLD), attended right standard (aRS), attended right deviant (aRD)) and the factor subject (22 levels), in order to assess the main effect of laterality, attention, and expectation violation, as well as the attention by expectation violation and laterality by expectation violation interactions
No difference was found in the detection accuracy between the two tasks; suggesting that participants were engaged in both attention conditions

Summary

Introduction

Expectation and attention both exert a strong influence on pain perception (e.g., Wiech et al, 2008) and the magnitude of pain-related neural responses (e.g., Dowman, 2007; Legrain et al, 2009b). Expectation violation and top-down attention have a similar effect on pain processing, as both unexpected and attended pain typically increase the amplitude of event-related potentials. The underlying neural mechanism of this common effect is unknown, one potential explanation lies in the theory of hierarchical predictive coding (Friston, 2005, 2008). This theory suggests that topdown and bottom-up signals are integrated by precision-dependent processes, where the precision or confidence afforded to ascending prediction error signals is encoded by postsynaptic gain (i.e., cortical gain control or excitation-inhibition balance; Feldman and Friston, 2010). Most frequently studied in the auditory domain (for reviews, see Näätänen et al, 2011, 2012), cortical mismatch responses have been observed for all sensory modalities, including somatosensation (e.g., Kekoni et al, 1997; Akatsuka et al, 2007b; Ostwald et al, 2012; Allen et al, 2016) and nociception (Hu et al, 2013a; Zhao et al, 2014; see Legrain et al, 2002, 2005)

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