Analysis of synchrony demonstrates ‘pain networks’ defined by rapidly switching, task-specific, functional connectivity between pain-related cortical structures

Abstract

Imaging studies indicate that experimental pain is processed in multiple cortical areas which are often characterized as a network. However, the functional connectivity within the network and the other properties of the network is poorly understood. Substantial evidence demonstrates that synchronous oscillations between two cortical areas may indicate functional connectivity between those areas. We test the hypothesis that cortical areas with pain-related activity are functionally connected during attention to a painful stimulus. We stimulated with a painful, cutaneous, laser stimulus and recorded the response directly from the cortical surface (electrocorticography--ECoG) over primary somatosensory (SI), parasylvian (PS), and medial frontal (MF) cortex through subdural electrodes implanted for treatment of epilepsy. The results demonstrate synchrony of ECoGs between cortical structures receiving input from nociceptors, as indicated by the occurrence of laser-evoked potentials (LEPs) and/or event-related desynchronization (ERD). Prior to the stimulus, directed attention to the painful stimulus consistently increased the degree of synchrony between SI and PS regions, as the subject anticipated the stimulus. After the laser stimulus, directed attention to the painful stimulus consistently increased the degree of synchrony between SI and MF cortex, as the subject responded by counting the stimulus. Therefore, attention to painful stimuli always enhanced synchrony between cortical pain-related structures. The pattern of this synchrony changed as the patient switched tasks from anticipation of the stimulus to counting the stimulus. These results are the first compelling evidence of pain networks characterized by rapidly switching, task-specific functional connectivity.

Synchronous with Your Feelings: Sensorimotor γ Band and Empathy for Pain

“…Indeed, changes of ␥-band neuronal oscillations clearly appear integral to a number of complex cognitive functions ranging from attention, language, memory and mental practice (Lutz et al, 2004; Bastiaansen and Hagoort, 2006) to crossmodal (Kanayama et al, 2009), and sensorimotor integration (Alonso et al, 1996;Wallace et al, 1996;Bauer et al, 2006;Szurhaj and Derambure, 2006). Relevant to the present study is that ␥-band activity plays a specific role in first-hand pain processing (Chen and Herrmann, 2001;Ohara et al, 2006;Gross et al, 2007;Hauck et al, 2007). In particular, a recent MEG study showed that pain-induced ␥-band oscillations in the primary somatosensory cortex were related to the subjective perception of pain stimulus intensity rather than to the objective intensity of the stimulus itself (Gross et al, 2007).…”

Attention to Painful Stimulation Enhances γ-Band Activity and Synchronization in Human Sensorimotor Cortex

“…Notably, these findings could be extended to pain processing in a recent study conducted in neurosurgical awake patients by demonstrating attention to painful laser stimuli to enhance intracranially recorded synchrony between distinct cortical pain-related regions (Ohara et al, 2006). The pattern of synchrony changed between the primary somatosensory cortex, the medial frontal cortex, and the insula as the patient switched from a distracted state to attention to the stimuli by counting the total number.…”

“…Top-down influences such as focused attention may act by modulating subthreshold oscillations in sensory assemblies and by enhancing the gain of oscillatory responses to stimuli that match stored contex-tual information Herrmann et al, 2004). Along the same lines, ␥-band oscillations might also play an integral role in pain perception and processing (Chen and Herrmann, 2001;Croft et al, 2002;Ohara et al, 2006).…”

Functional integration within the human pain system as revealed by Granger causality

“…The results of these studies showed nearly simultaneous pain-evoked activations in S1, S2 and ACC [Frot et al, 2008;Ohara et al, 2004;Ploner et al, 1999] which differ from more sequential activation patterns in other modalities and suggest a partly parallel organization of pain processing in the human brain. Other studies applied coherence analyses and showed pain-related changes in functional connectivity between brain areas related to pain [Llinas et al, 1999;Ohara et al, 2008;Ohara et al, 2006;Sarnthein and Jeanmonod, 2008]. However, temporal sequences and correlations do not directly imply information on causal relationships between neural activations.…”