Abstract
Neuroimaging technologies with an exceptional spatial resolution and noninvasiveness have become a powerful tool for assessing neural activity in both animals and humans. However, the effectiveness of neuroimaging for pain remains unclear partly because the neurovascular coupling during pain processing is not completely characterized. Our current work aims to unravel patterns of neurovascular parameters in pain processing. A novel fiber-optic method was used to acquire absolute values of regional oxy- (HbO) and deoxy-hemoglobin concentrations, oxygen saturation rates (SO2), and the light-scattering coefficients from the spinal cord and primary somatosensory cortex (SI) in 10 rats. Brief mechanical and electrical stimuli (ranging from innocuous to noxious intensities) as well as a long-lasting noxious stimulus (formalin injection) were applied to the hindlimb under pentobarbital anesthesia. Interhemispheric comparisons in the spinal cord and SI were used to confirm functional activation during sensory processing. We found that all neurovascular parameters showed stimulation-induced changes; however, patterns of changes varied with regions and stimuli. Particularly, transient increases in HbO and SO2 were more reliably attributed to brief stimuli, whereas a sustained decrease in SO2 was more reliably attributed to formalin. Only the ipsilateral SI showed delayed responses to brief stimuli. In conclusion, innocuous and noxious stimuli induced significant neurovascular responses at critical centers (e.g., the spinal cord and SI) along the somatosensory pathway; however, there was no single response pattern (as measured by amplitude, duration, lateralization, decrease or increase) that was able to consistently differentiate noxious stimuli. Our results strongly suggested that the neurovascular response patterns differ between brief and long-lasting noxious stimuli, and can also differ between the spinal cord and SI. Therefore, a use of multiple-parameter strategy tailored by stimulus modality (brief or long-lasting) as well as region-dependent characteristics may be more effective in detecting pain using neuroimaging technologies.
Highlights
While decades of discoveries using neuroimaging technologies have revealed rich and complex processes underlying various brain functions [1], the use of neuroimaging as an objective tool to quantify or measure pain has been questioned [2]
Several human studies using near infrared spectroscopy have demonstrated that thermal or electrical stimulations induce changes of hemoglobin concentrations at different brain regions [7,8,9]
A gradual decrease in SO2 appeared to be a unique pattern for formalin-induced sustained pain, which may be a biomarker candidate for long-lasting pain
Summary
While decades of discoveries using neuroimaging technologies have revealed rich and complex processes underlying various brain functions [1], the use of neuroimaging as an objective tool to quantify or measure pain has been questioned [2] This is because pain is a multifactorial subjective experience of the nociceptive inputs associated with one’s memories as well as emotional, pathological, genetic, and cognitive factors [3]. Animal studies become a necessary and important approach to address many of the physiological questions In this particular study, we aimed to answer the following questions: (i) how vascular hemoglobin concentrations and oxygenation change under various short-term mechanical and electrical stimuli as well as a long-lasting chemical stimulus; (ii) whether the nociception-induced hemoglobin-based parameters are contralateral or bilateral in the primary somatosensory cortex (SI) and/or spinal cord; and (iii) whether there exists a single parameter that is consistently associated with noxious stimuli
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