Reward and aversion processing in patients with post-traumatic stress disorder: functional neuroimaging with visual and thermal stimuli

Igor Elman,Mark Albanese,Lino Becerra,David Borsook,Jaymin Upadhyay,Daniel D Langleben

doi:10.1038/s41398-018-0292-6

Abstract

In patients with post-traumatic stress disorder (PTSD), a decrease in the brain reward function was reported in behavioral- and in neuroimaging studies. While pathophysiological mechanisms underlying this response are unclear, there are several lines of evidence suggesting over-recruitment of the brain reward regions by aversive stimuli rendering them unavailable to respond to reward-related content. The purpose of this study was to juxtapose brain responses to functional neuroimaging probes that reliably produce rewarding and aversive experiences in PTSD subjects and in healthy controls. The stimuli used were pleasant, aversive and neutral images selected from the International Affective Picture System (IAPS) along with pain-inducing heat applied to the dorsum of the left hand; all were administered during 3 T functional magnetic resonance imaging. Analyses of IAPS responses for the pleasant images revealed significantly decreased subjective ratings and brain activations in PTSD subjects that included striatum and medial prefrontal-, parietal- and temporal cortices. For the aversive images, decreased activations were observed in the amygdala and in the thalamus. PTSD and healthy subjects provided similar subjective ratings of thermal sensory thresholds and each of the temperatures. When 46 °C (hot) and 42 °C (neutral) temperatures were contrasted, voxelwise between-group comparison revealed greater activations in the striatum, amygdala, hippocampus and medial prefrontal cortex in the PTSD subjects. These latter findings were for the most part mirrored by the 44 vs. 42 °C contrast. Our data suggest different brain alterations patterns in PTSD, namely relatively diminished corticolimbic response to pleasant and aversive psychosocial stimuli in the face of exaggerated response to heat-related pain. The present findings support the hypothesis that brain sensitization to pain in PTSD may interfere with the processing of psychosocial stimuli whether they are of rewarding or aversive valence.

Highlights

Reward deficiency, that is to say, hypofunctionality of the brain reward circuitry manifested in the diminution of drives and in inability to experience joy or pleasure[1] is considered by some[2,3] to be the most specific diagnostic[4]feature of post-traumatic stress disorder (PTSD) documented in preclinical studies[5] along with behavioral[6,7] and neuroimaging[8,9] clinical research
Elman et al Translational Psychiatry (2018)8:240. With regard to the former possibility, individuals afflicted with reward deficiency may perceive their life as bland and unfulfilling and possess a character trait of novelty seeking[13,14], which could drive their engagement in stressogenic situations with an elevated potential for trauma exposure and subsequent PTSD15,16
Subjects Twelve subjects meeting the DSM-IV-TR criteria for PTSD, diagnosed via the Structured Clinical Interview for DSM-IV58 and Clinician-Administered PTSD Scale (CAPS)[59], and 12 mentally healthy subjects were recruited by advertisement

Summary

Introduction

That is to say, hypofunctionality of the brain reward circuitry manifested in the diminution of drives and in inability to experience joy or pleasure[1] is considered by some[2,3] to be the most specific diagnostic[4]feature of post-traumatic stress disorder (PTSD) documented in preclinical studies[5] along with behavioral[6,7] and neuroimaging[8,9] clinical research. With regard to the former possibility, individuals afflicted with reward deficiency may perceive their life as bland and unfulfilling and possess a character trait of novelty seeking[13,14], which could drive their engagement in stressogenic situations with an elevated potential for trauma exposure and subsequent PTSD15,16. This causality could run in the opposite direction[17]. Reward deficiency is caused by dampening reward circuitry neurotransmission by way of enhanced dopamine metabolism[26], its inhibited synthesis[27] or extracellular release[28,29] in conjunction with the reduction in dopamine receptors’ number[30] and activity[31,32]

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