Facial expressions, pain and nociception—are they related?
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www.nature.com/clinicalpractice/neuro Patients with dementia often have a diminished capacity to verbally report and accurately describe pain symptoms because of their cognitive impair- ment. 1 Thus, there is a need for the development of alternative, nonverbal ways to clinically assess pain in these patients. Observation of facial behaviors has been suggested as a clinically useful means of assessing pain in this popula- tion because of the unique facial expressions associated with pain compared with other affective states. 1 A recent publication by Kunz and colleagues explored the degree to which pain was facially expressed by patients with dementia, by use of controlled noxious stimuli and quantitative assessment of facial expressions. 1 The authors studied 42 patients with various types of dementia and 54 healthy, age-matched controls. Graded pressure stimulation was delivered to the forearm by use of a Fischer algometer. Each of the participants verbally rated the severity of their pain on a six-point Likert scale. In addi- tion, their facial expressions were video-taped, and the Facial Action Coding System was used to quantify the frequency and intensity of facial responses on a five-point Likert scale. As expected, the authors found that patients with dementia had a reduced capacity to verbally report their degree of pain that was highly corre- lated to the severity of their cognitive decline. However, these patients showed markedly greater frequency and increased intensity of typical facial reactions to pain in response to ‘pain-relevant’ and also ‘pain-irrelevant’ stimuli compared with controls. In other words, patients showed facial pain when there was no pain source, and if there was a pain source they showed excessive facial pain, which indicates that facial expressions of pain are augmented in patients with dementia and, thus, a poor marker for nociception. These findings were unexpected and, from a clinical perspective, limit the usefulness of facial expres- sions in patients with dementia as an accurate behavioral response to nociceptive stimuli. To better understand why these results occurred, it Facial expressions, pain and nociception—are they related? Elliott D Ross ED Ross is Professor of Neurology at the University of Oklahoma Health Sciences Center and Director of the Center for Alzheimer’s and Neurodegenerative Disorders at Oklahoma City VA Medical Center, Oklahoma City, OK, USA. Correspondence Oklahoma City VA Medical Center (11AZ) 921 NE 13 th Street Oklahoma City OK 73104 USA [email protected] Received 30 January 2008 Accepted 7 March 2008 Published online 22 April 2008 www.nature.com/clinicalpractice doi:10.1038/ncpneuro0791 is necessary to explore how facial expressions, pain and nociception are related to each other. Noxious stimuli, which cause physical injury to tissue, give rise to neural signals that are gener- ated by nocireceptors associated with thinly myelinated A-gamma fibers and unmyelinated C fibers that terminate in the dorsal horn of the spinal cord and equivalent structures in the brainstem. 2 Second-order neurons cross the midline and form the spinothalamic and quintothalamic tracts that project to various medial and lateral thalamic nuclei, which in turn project to various cortical regions of the forebrain for cognitive elaboration. In addition, a substantial percentage of spinothalamic and quintothalamic fibers project to the medial retic- ular formation of the brainstem and gain access to the forebrain and related limbic areas via indirect connections. 3 The understanding of how pain, as an experi- ential and behavioral phenomenon, is related to nociception has traditionally been hindered by two concepts: until the mid-1900s, the cerebral cortex was thought not to be involved directly with pain processing, and the intensity of noci- ception was thought to be tightly correlated to the intensity of the pain experience. 2,4 However, observations of the behavior of wounded soldiers in battle, 4 clinical studies of patients with focal lesions of the cerebrum, 5,6 and psychological experiments that manipulated the psychosocial milieu, financial rewards and expectations of healthy individuals, 7 as well as animal experi- ments, 8 have firmly established that nociception and the experiential and behavioral aspects of pain are, at best, poorly related to each other. For example, patients who have undergone prefrontal leucotomies for relief of intractable pain have normal nociceptive-pain thresholds with appropriate behavioral responses to acute noxious stimuli but show diminished anxiety, lack of emotional concern and inattentiveness to their intractable pain. 5 Pain asymbolia is an acquired clinical condition that is characterized by loss of emotional reactivity to threatening 304 NATURE CLINICAL PRACTICE NEUROLOGY JUNE 2008 VOL 4 NO 6 VIEWPOINT
Transcript of Facial expressions, pain and nociception—are they related?
www.nature.com/clinicalpractice/neuro
Patients with dementia often have a diminished capacity to verbally report and accurately describe pain symptoms because of their cognitive impair-ment.1 Thus, there is a need for the development of alternative, nonverbal ways to clinically assess pain in these patients. Observation of facial behaviors has been suggested as a clinically useful means of assessing pain in this popula-tion because of the unique facial expressions associated with pain compared with other affective states.1
A recent publication by Kunz and colleagues explored the degree to which pain was facially expressed by patients with dementia, by use of controlled noxious stimuli and quantitative assessment of facial expressions.1 The authors studied 42 patients with various types of dementia and 54 healthy, age-matched controls. Graded pressure stimulation was delivered to the forearm by use of a Fischer algometer. Each of the participants verbally rated the severity of their pain on a six-point Likert scale. In addi-tion, their facial expressions were video-taped, and the Facial Action Coding System was used to quantify the frequency and intensity of facial responses on a five-point Likert scale. As expected, the authors found that patients with dementia had a reduced capacity to verbally report their degree of pain that was highly corre-lated to the severity of their cognitive decline. However, these patients showed markedly greater frequency and increased intensity of typical facial reactions to pain in response to ‘pain-relevant’ and also ‘pain-irrelevant’ stimuli compared with controls. In other words, patients showed facial pain when there was no pain source, and if there was a pain source they showed excessive facial pain, which indicates that facial expressions of pain are augmented in patients with dementia and, thus, a poor marker for nociception. These findings were unexpected and, from a clinical perspective, limit the usefulness of facial expres-sions in patients with dementia as an accurate behavioral response to nociceptive stimuli. To better understand why these results occurred, it
Facial expressions, pain and nociception—are they related?Elliott D Ross
ED Ross is Professor of Neurology at the University of Oklahoma Health Sciences Center and Director of the Center for Alzheimer’s and Neurodegenerative Disorders at Oklahoma City VA Medical Center, Oklahoma City, OK, USA.
CorrespondenceOklahoma City VA Medical Center (11AZ) 921 NE 13th Street Oklahoma City OK 73104 USA [email protected]
Received 30 January 2008 Accepted 7 March 2008 Published online 22 April 2008
www.nature.com/clinicalpracticedoi:10.1038/ncpneuro0791
is necessary to explore how facial expressions, pain and nociception are related to each other.
Noxious stimuli, which cause physical injury to tissue, give rise to neural signals that are gener-ated by nocireceptors associated with thinly myelinated A-gamma fibers and unmyelinated C fibers that terminate in the dorsal horn of the spinal cord and equivalent structures in the brainstem.2 Second-order neurons cross the midline and form the spinothalamic and quintothalamic tracts that project to various medial and lateral thalamic nuclei, which in turn project to various cortical regions of the forebrain for cognitive elaboration. In addition, a substantial percentage of spinothalamic and quintothalamic fibers project to the medial retic-ular formation of the brainstem and gain access to the forebrain and related limbic areas via indirect connections.3
The understanding of how pain, as an experi-ential and behavioral phenomenon, is related to nociception has traditionally been hindered by two concepts: until the mid-1900s, the cerebral cortex was thought not to be involved directly with pain processing, and the intensity of noci-ception was thought to be tightly correlated to the intensity of the pain experience.2,4 However, observations of the behavior of wounded soldiers in battle,4 clinical studies of patients with focal lesions of the cerebrum,5,6 and psychological experiments that manipulated the psychosocial milieu, financial rewards and expectations of healthy individuals,7 as well as animal experi-ments,8 have firmly established that nociception and the experiential and behavioral aspects of pain are, at best, poorly related to each other. For example, patients who have undergone prefrontal leucotomies for relief of intractable pain have normal nociceptive-pain thresholds with appropriate behavioral responses to acute noxious stimuli but show diminished anxiety, lack of emotional concern and inattentiveness to their intractable pain.5 Pain asymbolia is an acquired clinical condition that is characterized by loss of emotional reactivity to threatening
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Competing interestsThe author declared no competing interests.
somatosensory, visual and auditory stimuli as a result of a lesion that involves, at minimum, the posterior insula.6 When presented with noxious or threatening stimuli, patients with pain asym-bolia will fail to respond appropriately to the threat by taking defensive measures and do not engage in avoidance behaviors on repeated presentation of the threatening stimuli. These patients are, however, able to describe in detail the threatening and noxious aspects of the stimuli and have intact and appropriate auto-nomic responses to them. In fact, if the skin of patients with this syndrome is cut sufficiently to draw blood, they may actually proffer their arm towards the examiner rather than with-drawing it. Similarly, soldiers on the battlefield who have extensive injuries may not complain of pain until they are brought to safety.4 Puppies that are raised in pain-free environments fail to learn to avoid noxious stimuli when exposed to them repeatedly as full-grown dogs; for example, when exposed to a lit match, these animals repeatedly burn their snouts trying to sniff at the flame despite showing an acute but very brief reflexive type of body jerk whenever their snouts are burned.8
Pain should, therefore, be viewed as a learned cognitive construct that has emotional, expe-riential, attentive, mnestic and psychosocial aspects.2–9 The clinical relationship of the experiential aspects of pain to actual noci-ception is highly variable because the behavioral components of pain (such as facial expres-sions) can be manipulated either consciously or subconsciously by individuals for various psychosocial purposes10,11 or may be altered by the presence of cerebral pathology.1,5,6 It should not be surprising, therefore, that patients with dementia have augmented painful expressions that are not reflective of the presence or intensity of nociception.1 Most probably, these patients have lost their ability to cognitively inhibit pain-typical facial expressions to both trivial and nociceptive stimuli because of their intellectual decline. From a behavioral perspective, this phenomenon has some characteristics that are similar to the acquired syndrome of pathological regulation of affect.12
The research findings by Kunz et al.1 provide important information that may help clinicians to correctly interpret the numerous behavioral changes that occur in patients with dementia. The fact that facial responses to noxious stimu-lation are preserved but not representative of the level of nociception means that care must be taken when a patient with dementia evinces expressions of facial pain; before an extensive evaluation is embarked on that could be poorly tolerated by the patient, the behavior must always be evaluated clinically to determine if it truly reflects a nociceptive process or represents a ‘false-positive’ behavior unrelated to a noci-ceptive process. In our experience of managing large numbers of patients with dementia in a longitudinal outpatient clinic, acute or subacute worsening of cognition or caregiver reports of increased agitation and confusion are the most helpful behavioral markers when deciding whether a patient has a complicating illness that needs urgent medical or surgical attention.
References1 Kunz M et al. (2007) The facial expression of pain in
patients with dementia. Pain 133: 221–2282 Schnitzler A and Ploner M (2000) Neurophysiology and
functional neuroanatomy of pain perception. J Clin Neurophysiol 17: 592–603
3 Bowsher D (1957) Termination of the central pain pathway in man: the conscious appreciation of pain. Brain 80: 606–621
4 Wall PD (1979) On the relationship of injury to pain. Pain 6: 253–264
5 Barber TX (1959) Toward a theory of pain: relief of chronic pain by prefrontal leucotomy, opiates, placebos, and hypnosis. Psychol Bull 56: 430–460
6 Berthier M et al. (1988) Asymbolia for pain: a sensory-limbic disconnection syndrome. Ann Neurol 24: 41–49
7 Weisenberg M (1984) Cognitive aspects of pain. In Textbook of Pain, 162–172 (Eds Wall PD and Melzack R) Edinburgh: Churchill-Livingstone
8 Melzack R and Scott TH (1957) The effects of early experience on the response to pain. J Comp Physiol Psychol 50: 155–161
9 Craig KD (1984) Emotional aspects of pain. In Textbook of Pain, 153–161 (Eds Wall PD and Melzack R) Edinburgh: Churchill-Livingstone
10 Williams AC (2002) Facial expression of pain: an evolutionary account. Behav Brain Sci 25: 439–488
11 Craig KD et al. (1991) Genuine suppressed and faked facial behavior during exacerbation of chronic low back pain. Pain 46: 161–171
12 Ross ED et al. (2007) Human facial expressions are organized functionally across the upper-lower facial axis. Neuroscientist 13: 433–446
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