Brief articleResponse-specific effects of pain observation on motor behavior☆
Introduction
We wince when a doctor’s needle breaks the skin, and even the mere prospect of a needle thrust into one’s flesh is enough to make many people cringe. Evidence from clinical and experimental research indicates that experiencing pain indeed influences the motor system, at levels ranging from reflex action in the spinal cord to modulation in pain-related areas of neocortex. Motor responses to pain are thought to serve a protective function, whether it is to withdraw from an immediately offensive noxious stimulus or to restrict the movement of an injured body part (Farina et al., 2003, Le Pera et al., 2001, Millan, 2002).
But what happens to our motor system when we see a doctor brandishing a needle at someone else? It is possible that pain observation, like pain itself, modulates motor behavior. These effects may even specifically enable appropriate movements, for example the readiness to withdraw the hand or to avoid touching an object. Such an influence of pain observation on motor responses would suggest that our representation of others’ pain is at least partly motoric. It would also support a perspective in which vicarious pain responses carry “selfish” heuristic advantages: motor representations accompanying pain observation could affect the observer’s responses to potentially harmful situations (Avenanti et al., 2005, Morrison, in press).
Despite accumulating evidence that experienced painful stimuli influence cortical motor systems, the nature of a similar influence during pain observation is currently unclear. Some research shows that pain observation inhibits hand muscles via the cortical motor system (Avenanti et al., 2005). This is proposed to reflect diminished cortical-level excitatory interference in favor of spinal reflexes (Valeriani et al., 2001), possibly by massively “switching off” motoneuron pools in the affected limb in order to reduce the range of potential motor responses (Leis et al., 2000). Another proposition is that motor readiness is facilitated by pain observation. Some evidence supporting this perspective comes from research showing that experiencing pain can reduce withdrawal reflex latencies via mechanisms of descending facilitation (Calejesan, Kim, & Zhuo, 2000), originating in cortical areas such as the anterior cingulate cortex which also utilize pain-related visual cues in a context-dependent manner (e.g., Iwata et al., 2005, Tang et al., 2005). A third possibility is that pain observation gives rise to complex patterns of facilitation and inhibition that vary according to the situation. Indeed, thus far research across species and methods has failed to demonstrate an invariant relationship between noxious stimulation and facilitation or inhibition of nociceptive or skeletomotor responses (Millan, 2002).
One approach to clarifying this in the case of pain observation is to measure the effect of pain observation on reaction times. No study to date has required participants to make overt movements following pain observation. In this experiment, we used a go/nogo reaction-time paradigm to explore how visual pain-related information contributes to the execution of motor responses at the behavioral level (Fig. 1). Reaction times were recorded after an interstimulus interval (ISI) of 100 or 500 ms, following 1-second video clips depicting needles pricking fingertips. Control clips depicted fingertips being touched by innocuous cotton buds, or sponges being touched with either needles or cotton buds. Button presses (approach movements) were compared to button releases (withdrawal movements; Wentura, Rothermund, & Bak, 2000). We predicted that pain observation would not only influence reaction times, but would do so in a context-dependent manner. That is, reaction times should decrease for withdrawal movements relative to approach movements, in response to viewing noxious compared to innocuous stimuli. This would support the hypothesis that pain observation influences the motor system in a response-specific manner.
Section snippets
Participants
Twenty-four right-handed female undergraduate volunteers (mean age 19) from the University of Manchester (N = 17) and University of Wales Bangor (N = 7), with normal or corrected-to-normal vision, participated in this study. Female students were recruited in order to reduce well-established gender variability that exists among pain, empathy, and fear measures. One subject’s data were excluded due to exceeding a limit of 20% errors.
Materials
There were 20 different hand movie clips, 10 of which depicted
Results
Mean errors did not exceed 3% in any of the eight conditions. The mean correct response times were submitted to a 2 × 2 × 2 × 2 repeated measures ANOVA with four within-subject factors: target, implement, ISI, and response type. There was a significant four-way interaction among these factors, F (1, 23) = 6.3, p = 0.02 (Fig. 2).
To investigate this interaction further, three-way ANOVAs were performed for the 100 and 500 ms ISI conditions separately. These analyses revealed a significant three-way
Discussion
This experiment demonstrates a specific influence of pain observation on overt motor responses. After viewing a video in which a needle pricked a finger, participants’ withdrawal movements were speeded and approach movements were slowed. However, this interaction between implement and response was only seen when the target of the needle was a hand, and not a non-body object (sponge). It was also seen only after a 500 ms interstimulus delay, but not after a shorter delay of 100 ms. In all other
Acknowledgments
The authors wish to thank Håkan Olausson, Giuseppe di Pellegrino, Marius Peelen, and Steven Tipper for their valuable comments on previous drafts.
References (23)
- et al.
Stimulus-driven modulation of motor-evoked potentials during observation of others’ pain
Neuroimage
(2006) - et al.
Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex
European Journal of Pain
(2000) - et al.
How do we perceive the pain of others?
Neuroimage
(2005) - et al.
Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain
Clinical Neurophysiology
(2001) Descending control of pain
Progress in Neurobiology
(2002)- et al.
Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain
Nature Neuroscience
(2005) - et al.
On the generality of the affective Simon effect
Cognition and Emotion
(2001) - et al.
Pain-related modulation of the human motor cortex
Neurological Research
(2003) The manifold nature of interpersonal relations: the quest for a common mechanism
Philosophical Transactions of the Royal Society of London: Biology
(2003)- et al.
Anterior cingulate cortical neuronal activity during perception of noxious thermal stimuli in monkeys
Journal of Neurophysiology
(2005)
Nociceptive fingertip stimulation inhibits synergistic motoneuron pools in the human upper limb
Neurology
Cited by (39)
Expertise and injury experience in professional skiers modulate the ability to predict the outcome of observed ski-related actions
2022, Psychology of Sport and ExerciseCitation Excerpt :It has been demonstrated that the observation of pain experience leads to motor system inhibition, similarly to what happens during the direct experience of pain (Avenanti, Minio-Paluello, Minio Paluello, Bufalari, & Aglioti, 2006, 2005; Avenanti, Minio-Paluello, Bufalari, & Aglioti, 2009; Avenanti, Minio-Paluello, Sforza, & Aglioti, 2009; Avenanti & Aglioti, 2006; Bucchioni et al., 2016; Bufalari, Aprile, Avenanti, Russo, & Aglioti, 2007; Farina, Tinazzi, Le Pera, & Valeriani, 2003; Valeriani et al., 2008). Furthermore, a pain resonance effect has been observed also at a behavioural level, with slower reaction times when participants are asked to press computer keys while observing painful compared to neutral scenes (Morrison, Poliakoff, Gordon, & Downing, 2007). These findings have been interpreted advocating the activation in the observer of a pain-resonant sensorimotor representation of the observed action.
Dynamic construction of the neural networks underpinning empathy for pain
2016, Neuroscience and Biobehavioral ReviewsCitation Excerpt :In the experience of pain, the cingulate cortex is known to participate in response selection, motor learning and motor planning (Peyron et al., 2000). This is possible thanks to the interaction between the action and pain systems that occurs during actual noxious stimulation (Farina et al., 2003; Perini et al., 2013; Svensson et al., 2003) as well as during the observation of others in painful situations (Avenanti et al., 2005; Avenanti et al., 2009; Avenanti et al., 2006; Morrison et al., 2007a; Morrison et al., 2007b). The above interaction might be mediated by ACC which is reciprocally connected with high order frontal regions (e.g., lateral prefrontal cortex) and other motor-related areas (Paus, 2001).
Grasping the pain: Motor resonance with dangerous affordances
2012, Consciousness and CognitionCitation Excerpt :Thus, having to witness pain being inflicted on others led to a specific corticospinal inhibition, similar to the way in which pain was directly-experienced (e.g., Farina, Tinazzi, Le Pera, & Valeriani, 2003; Le Pera et al., 2001); this suggested a resonant activation of pain representations in the onlooker’s sensorimotor system. Not only neural, but also behavioral evidence (Morrison, Poliakov, Gordon, & Downing, 2007) has demonstrated a specific influence on overt motor responses when pain is observed. More specifically, observing a video of a needle penetrating a hand accelerated withdrawal movements (key releases) and slowed approach movements (key presses); this difference was not present when participants observed a cotton bud touching a hand or when it was a sponge, rather than a hand, being penetrated or touched by either a needle or cotton bud.
A satisficing and bricoleur approach to sensorimotor cognition
2012, BioSystemsCitation Excerpt :There are many other examples in the interactions between color and shape or shape and position processing (Janssen et al., 2008; Ponce et al., 2011). As for the modulated principle, there are studies showing that, for example, pain observation modulates the motor system by modifying movements and motor plans, illustrating that visual information about pain is used to facilitate appropriate behavioral responses (Morrison et al., 2007). Finally, and in relation with the open principle, the interaction with an object cannot be understood without considering the complete coupling between the brain and the object, including the object, the sensorimotor processing and the stored knowledge on the object.
- ☆
This manuscript was accepted under the editorship of Jacques Mehler.