Cross-frequency coupling in deep brain structures upon processing the painful sensory inputs

Abstract

Cross-frequency coupling has been shown to be functionally significant in cortical information processing, potentially serving as a mechanism for integrating functionally relevant regions in the brain. In this study, we evaluate the hypothesis that pain-related gamma oscillatory responses are coupled with low-frequency oscillations in the frontal lobe, amygdala and hippocampus, areas known to have roles in pain processing. We delivered painful laser pulses to random locations on the dorsal hand of five patients with uncontrolled epilepsy requiring depth electrode implantation for seizure monitoring. Two blocks of 40 laser stimulations were delivered to each subject and the pain-intensity was controlled at five in a 0–10 scale by adjusting the energy level of the laser pulses. Local-field-potentials (LFPs) were recorded through bilaterally implanted depth electrode contacts to study the oscillatory responses upon processing the painful laser stimulations. Our results show that painful laser stimulations enhanced low-gamma (LH, 40–70 Hz) and high-gamma (HG, 70–110 Hz) oscillatory responses in the amygdala and hippocampal regions on the right hemisphere and these gamma responses were significantly coupled with the phases of theta (4–7 Hz) and alpha (8–12 Hz) rhythms during pain processing. Given the roles of these deep brain structures in emotion, these findings suggest that the oscillatory responses in these regions may play a role in integrating the affective component of pain, which may contribute to our understanding of the mechanisms underlying the affective information processing in humans.

Oscillatory EEG activity induced by conditioning stimuli during fear conditioning reflects Salience and Valence of these stimuli more than Expectancy

“…Gamma EEG oscillations that occur in the human cortex, hippocampal formation and amygdala may be related to theta rhythms through cross frequency coupling as the theta rhythm modulates the gamma rhythm during the formation of declarative memories and the response to stimuli of negative Valence, such as pain (Fell et al, 2003; Liu et al, 2015a,b). These stimuli evoke both theta and gamma frequency activity over central, parietoinsular and medial Frontal sites, which may be connected to the hippocampus through the entorhinal cortex (Van and Pandya, 1975a,b; Aggleton et al, 1980).…”

Enhanced Gamma Oscillatory Activity in Rats with Chronic Inflammatory Pain

“…Although there are several studies on gamma oscillations in experimental brief and tonic pain in healthy human beings and in normal rats (Croft et al, 2002; Gross et al, 2007; Wang et al, 2011; Hu et al, 2014; Liu et al, 2015b,a; Schulz et al, 2015; Li et al, 2016), as well as convert pain in patients with chronic disorders of consciousness (Naro et al, 2016), knowledge about the spontaneous and task-free gamma oscillatory activity in pathological, long-lasting chronic pain state are still in expectation. Our present study found that ECoG gamma activity increased under chronic inflammatory pain condition in a CFA monoarthritis model of rats.…”

“…It has been reported that gamma band activation participates in pain perception. The power of gamma oscillations increases after brief nociceptive laser stimulations in healthy human beings (Gross et al, 2007; Tiemann et al, 2010; Schulz et al, 2011; Zhang et al, 2012; Hu et al, 2014; Liu et al, 2015a,b) and in normal rats (Wang et al, 2011), indicating that gamma oscillations are related to experimental acute pain lasting for milliseconds to seconds. Such gamma activity is focused on somatosensory cortex and positively correlated with the perceived pain intensity measured by the subjective rating of pain sensation on human beings (Gross et al, 2007; Zhang et al, 2012; Hu et al, 2014; Liu et al, 2015a) and with convert pain processing in patients with chronic disorders of consciousness (Naro et al, 2016).…”

“…Such gamma activity is focused on somatosensory cortex and positively correlated with the perceived pain intensity measured by the subjective rating of pain sensation on human beings (Gross et al, 2007; Zhang et al, 2012; Hu et al, 2014; Liu et al, 2015a) and with convert pain processing in patients with chronic disorders of consciousness (Naro et al, 2016). Recent recordings from deep brain structures on human beings discovered that laser nociceptive stimulation on skin could induce gamma activation in brain regions like the parasylvian, the thalamus, right amygdala, and the hippocampus (Liu et al, 2015a,b). …”

Electroacupuncture Treatment Alleviates the Remifentanil-Induced Hyperalgesia by Regulating the Activities of the Ventral Posterior Lateral Nucleus of the Thalamus Neurons in Rats

“…In addition, cross-frequency coupling has functional significance in cortical information processing, thereby contributing to the integration of relevant regions in the brain [ 68 ]. In human beings, painful laser stimulation enhance gamma oscillatory responses in the pain-related amygdala and hippocampal regions, and these gamma responses are significantly coupled with the phases of theta and alpha rhythms during pain processing [ 69 ]. Painful cutaneous laser stimuli also induce event-related gamma band activity in the lateral thalamus in humans, and thalamic cross-frequency coupling analysis indicates that the phase of the lower frequency activity (theta to beta) modulates the amplitude of the higher frequency activity (low and high gamma) more strongly during the cutaneous laser stimuli [ 70 ].…”