Functional dissociation of stimulus intensity encoding and predictive coding of pain in the insula.

Stephan Geuter,Falk Eippert,Christian Büchel,Sabrina Boll

doi:10.7554/elife.24770

Abstract

The computational principles by which the brain creates a painful experience from nociception are still unknown. Classic theories suggest that cortical regions either reflect stimulus intensity or additive effects of intensity and expectations, respectively. By contrast, predictive coding theories provide a unified framework explaining how perception is shaped by the integration of beliefs about the world with mismatches resulting from the comparison of these beliefs against sensory input. Using functional magnetic resonance imaging during a probabilistic heat pain paradigm, we investigated which computations underlie pain perception. Skin conductance, pupil dilation, and anterior insula responses to cued pain stimuli strictly followed the response patterns hypothesized by the predictive coding model, whereas posterior insula encoded stimulus intensity. This novel functional dissociation of pain processing within the insula together with previously observed alterations in chronic pain offer a novel interpretation of aberrant pain processing as disturbed weighting of predictions and prediction errors.

Highlights

Classic bottom-up views construe perception as a feedforward stream of sensory information that is passed along the neural hierarchy from receptors to high-level brain regions (Hubel and Wiesel, 1959)
Other neuroimaging studies have shown that stimulus-response functions differ between brain regions (Davis et al, 1998; Coghill et al, 1999; Apkarian et al, 2001; Bornhovd et al, 2002; Davis et al, 2002; Porro et al, 2004) and that brain activation is modulated by concurrent task demands (Bantick et al, 2002; Valet et al, 2004; Wiech et al, 2005; Seminowicz and Davis, 2007; Villemure and Bushnell, 2009)
This pain prediction error (PE) is motivated by previous work (Egner et al, 2010; Buchel et al, 2014; Summerfield and de Lange, 2014), by the observation that PE for warm stimuli have topographies distinct from PE for pain (Ploghaus et al, 2000; Zeidan et al, 2015), and findings suggesting that reward and aversive PE are encoded by different neuronal populations (Yacubian et al, 2006; Belova et al, 2007; Seymour et al, 2007; Fiorillo, 2013)

Summary

Introduction

Classic bottom-up views construe perception as a feedforward stream of sensory information that is passed along the neural hierarchy from receptors to high-level brain regions (Hubel and Wiesel, 1959). Other neuroimaging studies have shown that stimulus-response functions differ between brain regions (Davis et al, 1998; Coghill et al, 1999; Apkarian et al, 2001; Bornhovd et al, 2002; Davis et al, 2002; Porro et al, 2004) and that brain activation is modulated by concurrent task demands (Bantick et al, 2002; Valet et al, 2004; Wiech et al, 2005; Seminowicz and Davis, 2007; Villemure and Bushnell, 2009) These theories cannot explain the reduction in sensory cortical activity for expected compared to unexpected stimuli

Methods

Results

Conclusion