Brain correlates of subjective reality of physically and psychologically induced pain

Abstract

Meaningful behavior requires successful differentiation of events surfacing from one's mind from those arising from the external world. Such judgements may be especially demanding during pain because of the strong contribution from psychological factors to this experience. It is unknown how the subjective reality of pain (SRP) is constructed in the human brain, and neuronal mechanisms of the subjective reality are poorly understood in general. To address these questions, 14 suggestion-prone healthy subjects rated reality of pain that was induced either by laser pulses to the skin or by hypnotic suggestion during functional MRI. Both pain states were associated with activation of the brain's pain circuitry. During laser stimulation, the sensory parts of this circuitry were activated more strongly, and their activation strengths correlated positively with the SRP. During suggestion-induced pain, the reality estimates were lower and correlated positively with activation strengths in the rostral and perigenual anterior cingulate cortex and in the pericingulate regions of the medial prefrontal cortex; a similar trend was evident during laser-induced pain. These findings support the view that information about sensorydiscriminative characteristics of pain contributes to the SRP. Differences in such information between physically and psychologically induced pain, however, could be quantitative rather than qualitative and therefore insufficient for judging the reality of pain without knowledge about the source of this information. The medial prefrontal cortex is a likely area to contribute to such source monitoring.functional MRI ͉ suggestion ͉ hypnosis ͉ human ͉ cortex E vents surfacing from one's mind are usually differentiated from those arising from the external world by the subjective experience of reality. Ability to differentiate real and imaginal percepts, however, can be distorted in patients suffering from various organic and functional brain disorders and occasionally even in healthy subjects (1-3).Brain correlates of pain are affected by various psychological factors (4-7). According to recent brain imaging studies, painrelated brain areas can be activated without any physical stimulus, solely by cognitive cues (7-9). It remains unknown, however, how real the subject's experiences of such a psychologically induced pain are, and how the subjective reality of pain (SRP) is constructed in the human brain. Because the clarity of a percept likely affects the experience of its reality, and because both real and hallucinatory percepts may be associated with activation of sensory brain areas (10, 11), we hypothesized that a neuronal system subserving the SRP should involve components that process pain-related sensory-discriminative information, i.e., the primary and secondary somatosensory cortices and the posterior insula (12, 13). We also expected this system to include brain regions such as the perigenual anterior cingulate cortex (pACC) (14) that are able to support source monitoring, because a failure to differ...

Cortical involvement during the description of head pain

“…Higher levels of activation were found with physically induced pain with respect to hypnotically induced pain, maybe owing to the more intense pain experience in the former condition [3,4]. In our research, the clusters of activation during description of head pain agree very closely with the results of the aforementioned studies [3,4], providing further evidence that brain regional activation within the pain circuitry is specifically involved in the subjective reality of pain. While mere imagining pain (the presence of a noxious heat stimulus) yielded only a minimal activation of the pain network in the study of Derbyshire et al [3], our preliminary findings (which need to be confirmed) suggest that remembering and describing the subjective experience of a recurrent pain may enhance cortical involvement, maybe through stronger emotional mechanisms.…”

“…In two recent studies [3,4] aimed at investigating the subjective reality of pain, functional magnetic resonance imaging revealed significant changes during a hypnotically induced pain experience -in the absence of any noxious stimulus -in the ACC, thalamus, insula, prefrontal and parietal cortices: this activation pattern was similar to that observed during pain from nociceptive sources.…”

“…Then, anticipation of pain may, itself, induce changes in brain nociceptive networks [10]. Moreover, recent experimental evidence has been provided, by means of functional magnetic resonance imaging, of a strict similarity in the processing of both hypnotically and physically induced experience of pain; the subjective dimension of pain (in the absence of any noxious stimulus) seems to involve brain regions (ACC, thalamus, insula, cerebellum, prefrontal and parietal cortices) variously described as belonging to the pain network [3,4]. Higher levels of activation were found with physically induced pain with respect to hypnotically induced pain, maybe owing to the more intense pain experience in the former condition [3,4].…”

“…Moreover, recent experimental evidence has been provided, by means of functional magnetic resonance imaging, of a strict similarity in the processing of both hypnotically and physically induced experience of pain; the subjective dimension of pain (in the absence of any noxious stimulus) seems to involve brain regions (ACC, thalamus, insula, cerebellum, prefrontal and parietal cortices) variously described as belonging to the pain network [3,4]. Higher levels of activation were found with physically induced pain with respect to hypnotically induced pain, maybe owing to the more intense pain experience in the former condition [3,4]. In our research, the clusters of activation during description of head pain agree very closely with the results of the aforementioned studies [3,4], providing further evidence that brain regional activation within the pain circuitry is specifically involved in the subjective reality of pain.…”

“…Also, two diagnostic categories (migraine and facial pain) were joined and studied together: the lack of differences between the two groups may be due to the small sample size again. Nevertheless, it seems that the same cortical areas within the pain network are involved in the subjective reality of pain, independently from its type [3,4].…”