Affective modulation of nociception at spinal and supraspinal levels JAMIE L. RHUDY, AMY E. WILLIAMS, KLANCI M. MCCABE, MARY ANH THU ` V. NGUYE ˆ  N, and PHILIP RAMBO Department of Psychology, The University of Tulsa, Tulsa, Oklahoma, USA Abstract This study was designed to examine the effect of emotion on the nociceptive ﬂexion reﬂex and pain ratings. To do so, 28 participants viewed pictures varying in emotional valence (unpleasant, neutral, pleasant) and electric stimulations were delivered during and in between pictures. Biceps femoris EMG resulting from the stimulations was used to quantify the nociceptive ﬂexion reﬂex (spinal nociception), and pain ratings to the stimulations were used as an evaluative measure of supraspinal nociception. Manipulation checks suggested that pictures effectively manipulated emotion. Moreover, nociceptive ﬂexion reﬂex magnitudes and pain ratings were modulated in a parallel manner. Specifically, viewing unpleasant pictures enhanced the nociceptive ﬂexion reﬂex and pain, whereas viewing pleasant pictures inhibited the reﬂex and pain. Analyses suggested that emotional valence, but not arousal, mediated the effects of pictures. Descriptors: Motivation, Appetitive, Defensive, Shock, NFR, R3 Reﬂex Pain is a complex, subjective experience not simply determined by the extent of noxious stimulation or nociception (neural transmission that may ultimately lead to subjective pain). Many factors are believed to inﬂuence the perception of pain, one of which is emotion. Unfortunately, few well-designed experimental studies have examined this issue, and most fail to: (a) use stand- ardized emotional stimuli, (b) include adequate manipulation checks for emotion-induction, and/or (c) test a comprehensive model of emotion (e.g., Haslam, 1966; Hill, Flanary, Kornetsky, & Wikler, 1952; Smith & Wolpin, 1989; Weaver & Zillmann, 1994; Westcott & Horan, 1977; Worthington, 1978). Moreover, little is known about the effect of emotion on human nociception at varying levels of the neuraxis. Most research has focused on subjective pain (or voluntary pain behaviors) that involve con- scious, supraspinally mediated evaluation of the noxious event. It is assumed that affective processes can modulate nociception at the spinal level; however, this hypothesis has yet to be addressed. Emotion is believed to be organized around two opponent motive systems. The defensive system is activated by harmful or potentially harmful stimuli (e.g., predator, electric shock, cue predicting threat) and results in avoidance behaviors and neg- ative affect. The appetitive system is activated by survival- enhancing stimuli (e.g., sex, ingestion, caregiving) and results in approach behaviors and positive affect. The motivational prim- ing theory (Lang, 1995; Lang, Bradley, & Cuthbert, 1992) argues that activation of a system primes (and thus potentiates) subse- quent responses emanating from that system, while inhibiting responses from the opposing system. Supporting this, several laboratories (Grillon, Ameli, Merikangas, Woods, & Davis, 1993; Jansen & Frijda, 1994; Lang, Bradley, & Cuthbert, 1990; Vrana, Spence, & Lang, 1988) have shown that priming the de- fensive system using unpleasant stimuli leads to potentiation of the acoustic startle reﬂex (a defensive response), whereas priming the appetitive system with pleasant stimuli leads to startle reﬂex inhibition. If the motivational priming theory is correct, then similar effects should be observed when other defensive reﬂexes are probed, with an opposite pattern for appetitive reﬂexes. Un- fortunately, research extending the motivational priming theory to other reﬂexes has been limited (cf. Benning, Patrick, & Lang, 2004; Bonnet, Bradley, Lang, & Requin, 1995). The Nociceptive Flexion Reﬂex: A Measure of Human Spinal Nociception The nociceptive ﬂexion reﬂex is a defensive response that allows withdrawal from a noxious stimulus (Skljarevski & Ramadan, 2002). This reﬂex can be elicited by electric stimulation of the sural nerve that activates primary nociceptors (Ad and C ﬁbers), resulting in the transmission of a nociceptive signal to the spinal cord that in turn elicits a withdrawal response in the leg. The stimulation intensity necessary to reliably elicit the nociceptive ﬂexion reﬂex (i.e., threshold) correlates with subjective report of pain threshold, and the amplitude of the nociceptive ﬂexion reﬂex correlates with subjective pain intensity (Chan & Dallaire, 1989; Guieu, Blin, Pouget, & Serratrice, 1992). Supraspinal regions are The authors would like to thank Jennifer Russell and three anony- mous reviewers for their helpful comments on an earlier draft of this article. Address reprint requests to: Jamie L. Rhudy, Ph.D., The University of Tulsa, Department of Psychology, 600 South College, Tulsa, OK 74104, USA. E-mail: jamie-rhudy@utulsa.edu. Psychophysiology, 42 (2005), 579–587. Blackwell Publishing Inc. Printed in the USA. Copyright r 2005 Society for Psychophysiological Research DOI: 10.1111/j.1469-8986.2005.00313.x 579