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The Journal of Neuroscience, January 28, 2004, 24(4):964-971; doi:10.1523/JNEUROSCI.1222-03.2004

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Behavioral/Systems/Cognitive
Perceptual Correlates of Nociceptive Long-Term Potentiation and Long-Term Depression in Humans

Thomas Klein,^1,2 * Walter Magerl,^1 * Hanns-Christian Hopf,² Jürgen Sandkühler,³ and Rolf-Detlef Treede¹

¹Institute of Physiology and Pathophysiology, Johannes Gutenberg University, D-55099 Mainz, Germany, ²Department of Neurology, Johannes Gutenberg University, D-55101 Mainz, Germany, and ³Brain Research Institute, Vienna University Medical School, A-1090 Vienna, Austria

Long-term potentiation (LTP) and long-term depression (LTD) of synaptic strength are ubiquitous mechanisms of synaptic plasticity, but their functional relevance in humans remains obscure. Here we report that a long-term increase in perceived pain to electrical test stimuli was induced by high-frequency electrical stimulation (HFS) (5 x 1 sec at 100 Hz) of peptidergic cutaneous afferents (27% above baseline, undiminished for >3 hr). In contrast, a long-term decrease in perceived pain (27% below baseline, undiminished for 1 hr) was induced by low-frequency stimulation (LFS) (17 min at 1 Hz). Pain testing with punctate mechanical probes (200 µm diameter) in skin adjacent to the HFS–LFS conditioning skin site revealed a marked twofold to threefold increase in pain sensitivity (secondary hyperalgesia, undiminished for >3 hr) after HFS but also a moderate secondary hyperalgesia (30% above baseline) after strong LFS. Additionally, HFS but not LFS caused pain to light tactile stimuli in adjacent skin (allodynia). In summary, HFS and LFS stimulus protocols that induce LTP or LTD in spinal nociceptive pathways in animal experiments led to similar LTP- and LTD-like changes in human pain perception (long-term hyperalgesia or hypoalgesia) mediated by the conditioned pathway. Additionally, secondary hyperalgesia and allodynia in adjacent skin induced by the HFS protocol and, to a minor extent, also by the LFS protocol, suggested that these perceptual changes encompassed an LTP-like heterosynaptic facilitation of adjacent nociceptive pathways by a hitherto unknown mechanism.

Key words: pain; hyperalgesia; central sensitization; spinal cord; neuropathic pain; pain memory

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Received April 23, 2003; revised November 10, 2003; accepted November 17, 2003.

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