Lamina‐specific population encoding of cutaneous signals in the spinal dorsal horn using multi‐electrode arrays

• Published in: The Journal of physiology Vol. 597; no. 2; pp. 377 - 397
• Main Authors: Greenspon, Charles M., Battell, Emma E., Devonshire, Ian M., Donaldson, Lucy F., Chapman, Victoria, Hathway, Gareth J.
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 01.01.2019; John Wiley and Sons Inc
• Subjects: Aluminum; Animals; Capsaicin - pharmacology; Central nervous system; Dorsal horn; Electric Stimulation; Electrical stimuli; Electrodes; Hot Temperature; Innervation; Male; Morphine; multi‐electrode array; Neuroethology; Pain perception; Phenotypes; Rats, Sprague-Dawley; Rodents; Somatosensory systems; Spinal cord; Spinal Cord Dorsal Horn - physiology; Techniques for Physiology; Touch; Somatosensory systems; Dorsal horn; multi-electrode array
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP277036

Key points Traditional, widely used in vivo electrophysiological techniques for the investigation of spinal processing of somatosensory information fail to account for the diverse functions of each lamina. To overcome this oversimplification, we have used multi‐electrode arrays, in vivo, to simultaneously record neuronal activity across all laminae of the spinal dorsal horn. Multi‐electrode arrays are sensitive enough to detect lamina‐ and region‐specific encoding of different subtypes of afferent fibres and to detect short‐lived changes in synaptic plasticity as measured by the application of cutaneous electrical stimulation of varying intensity and frequency. Differential encoding of innocuous and noxious thermal and mechanical stimuli were also detected across the laminae with the technique, as were the effects of the application of capsaicin. This new approach to the study of the dorsal spinal cord produces significantly more information per experiment, permitting accelerated research whilst also permitting the effects of pharmacological tools to modulate network responses. The dorsal horn (DH) of the spinal cord is a complex laminar structure integrating peripheral signals into the central nervous system. Spinal somatosensory processing is commonly measured electrophysiologically in vivo by recording the activity of individual wide‐dynamic‐range neurons in the deep DH and extrapolating their behaviour to all cells in every lamina. This fails to account for the specialized processes that occur in each lamina and the considerable heterogeneity in cellular phenotype within and between laminae. Here we overcome this oversimplification by employing linear multi‐electrode arrays (MEAs) in the DH of anaesthetized rats to simultaneously measure activity across all laminae. The MEAs, comprising 16 channels, were inserted into the lumbar dorsal horn and peripheral neurons activated electrically via transcutaneous electrodes and ethologically with von Frey hairs (vFHs) or an aluminium heating block. Ascending electrical stimuli showed fibre thresholds with distinct dorsoventral innervation profiles. Wind up was observed across the DH during the C‐fibre and post‐discharge latencies following 0.5 Hz stimulation. Intrathecal application of morphine (5 ng/50 μl) significantly reduced Aδ‐ and C‐fibre‐evoked activity in deep and superficial DH. Light vFHs (≤10 g) predominantly activated intermediate and deep laminae whereas noxious vFHs (26 g) also activated the superficial laminae. Noxious heat (55°C) induced significantly greater activity in the superficial and deep laminae than the innocuous control (30°C). The application of these arrays produced the first description of the processing of innocuous and noxious stimuli throughout the intact DH. Key points Traditional, widely used in vivo electrophysiological techniques for the investigation of spinal processing of somatosensory information fail to account for the diverse functions of each lamina. To overcome this oversimplification, we have used multi‐electrode arrays, in vivo, to simultaneously record neuronal activity across all laminae of the spinal dorsal horn. Multi‐electrode arrays are sensitive enough to detect lamina‐ and region‐specific encoding of different subtypes of afferent fibres and to detect short‐lived changes in synaptic plasticity as measured by the application of cutaneous electrical stimulation of varying intensity and frequency. Differential encoding of innocuous and noxious thermal and mechanical stimuli were also detected across the laminae with the technique, as were the effects of the application of capsaicin. This new approach to the study of the dorsal spinal cord produces significantly more information per experiment, permitting accelerated research whilst also permitting the effects of pharmacological tools to modulate network responses.