Our tactile world is infinitely rich: a cold breeze, a sharp poke, raindrops, or a mother’s gentle caress all impose mechanical forces on our skin, and yet we encounter no difficulty in telling them apart and can react differently to each. How do we recognize and interpret the myriad of tactile stimuli to perceive our physical world? Aristotle classified touch, along with vision, hearing, smell, and taste, as one of the five main senses. Yet among these five senses touch remains particularly underexplored. We still lack a detailed understanding of the neuronal circuits of touch, from skin to the brain, and how different brain networks contribute to our tactile experiences.
The anatomical substrate of innocuous touch perception is rooted in the intricate innervation patterns of specialized and highly diverse peripheral sensory neurons termed Low-Threshold Mechanoreceptors (LTMRs). These at one end innervate our skin and on the other innervate several different structures of our central nervous system. The historical view of touch information processing has emphasized the “direct pathway,” in which subsets of LTMRs that innervate skin send direct projections via the dorsal horn to the brainstem which then connect to the brain’s cortex. In this classic, but severely simplified, “labeled line” model, touch integration and processing begins in the cortex, with subcortical regions, such as the spinal cord, serving as simple relay stations. However, decades of work have shown that only a subset of LTMRs extend these direct projections to the brain, while all LTMRs exhibit projections that terminate in the spinal cord in a highly organized manner. Thus, “indirect” spinal cord networks are likely to play a critical role as gatekeepers in conveying processed and perceptually relevant touch information from the skin to the brain.
In support of this model, Abraira et. al. report an array of mouse genetic tools that illuminate the cellular and synaptic landscape of the spinal cord region that receives LTMR information and thus provide the first blueprint of the intricate spinal cord networks that influence the way that we perceive our tactile world. The authors found that this LTMR-recipient zone of the spinal cord exhibits an remarkable complexity of intricate neuronal connections, with at least 11 different classes of local interneurons that receive and process convergent information from different kinds of LTMRs as well as direct descending input from the brain’s cortex. Thus, each spinal cord neuron has the potential to serve as functionally distinct integrators of tactile information from the skin as well as internal states set forth by the cortex. Their work further shows, that these intricate spinal cord connections influence the activity of ascending spinal cord projection neurons that carry information from the spinal cord to the brain in ways that are likely essential for proper tactile detection and discrimination.
Collectively this study supports an alternative “integrative” model of touch information processing in which tactile integration and perception begins at the level of the spinal cord to influence the way we perceive our tactile world. In this emerging view, the spinal cord seems to play a key role as gatekeeper when processing touch information from the skin and integrating it with descending information from the brain. The authors speculate that this is likely the reason why our experience of touch can often be conditioned by context. The brain does not simply encode sensory information, but it integrates it with contextual information such as reward, expectation, attention, and motor action. This contextual information is likely to be fed back to these spinal cord networks via these descending connections to influence the way these networks process touch information emanating from the skin.
Moving forward, in laying down this blueprint of connections, this research will not only reveal key concepts of tactile information coding but may also shed light on how these spinal cord networks integrate information about pain, itch, temperature and proprioceptive information all of which are also conveyed through our skin.
About Victoria E. Abraira
Victoria completed her PhD training at Harvard Medical School in 2009 studying under the mentorship of Dr. Lisa Goodrich. Her graduate thesis used molecular-genetic approaches to uncover genes and pathways necessary for inner ear morphogenesis and the development of hindbrain auditory nuclei in mice. Victoria is now a Goldenson Post-Doctoral Fellow at Harvard Medical School in the lab of Dr. David Ginty using mouse molecular genetics to understand our sense of touch.
Abraira, Victoria E., Emily D. Kuehn et al. (2017) The Cellular and Synaptic Architecture of the Mechanosensory Dorsal Horn. Cell, Volume 168 , Issue 1 , 295 – 310.e19. Open Access – free access to the full article
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