All knowledge about the world is perceived through our sensory systems which consist of peripheral sensory organs, sensory nerves and central nervous system (CNS). In principle a sensation is classified according to its modality, a kind of energy inducing physiological transduction in a specific group of sensory organs. For example, in the somatosensory systems, each mode of touch-pressure, temperature or pain is sensed by independent sensory endings of primary afferent neurons and conducted to the specific cortical locus as nerve impulses, but integrated thereafter as a whole. Although it has been anticipated that the peripheral sensory nerve endings would become photosensitive with the ectopic expression of photoreceptive molecules, it has never been proved with the mammalian systems. Could the animal sense light on its skin if the peripheral sensory nerve endings are photosensitive? In one of transgenic rat lines which express channelrhodopsin-2 (ChR2), one of algal photoreceptive molecules (1, 2), the light is sensed by skin through the touch-pressure sensitive nerve endings. We provided evidences for the first time that the sensory modality of the somatosensory system can be modified so as to be also reactive to light even in the rat. We have previously generated several lines of transgenic rats which express ChR2 under regulation of Thy1.2 promoter (3). The transgene expression was variable from line to line, being dependent on the integration sites in chromosomes and/or the number of inserted copies (4). In one of these transgenic rat lines, W-TChR2V4, ChR2 was specifically expressed in a subpopulation of mechanoreceptive neurons in the dorsal root ganglion (DRG) but not in the small-sized neurons which are involved in nociception. Furthermore, ChR2 is also expressed in their peripheral nerve endings such as those innervating Merkel corpuscles and Meissner corpuscles, which are involved in the touch sense. Indeed, this transgenic rat showed a sensory-evoked behavior in response to blue flash light on their plantar skin as if it were touched by something. However, it ignores red light that is not sensed by ChR2. It is thus concluded that the rat has acquired an unusual sensory modality that it senses light at skin (5). We also identified the expression of ChR2 in the peripheral endings of trigeminal mechanoreceptive neurons which innervate whisker follicles. Is a whisker-related sensory perception induced by the photostimulation of their follicles? To test this, the barrel cortex responses were examined using electrophysiological recordings and functional magnetic resonance imaging (fMRI). Under anesthesia with urethane, the whiskers were trimmed and connected with optic fibers of which other endings were connected to LEDs. Pulsative irradiation of blue LED light was used as a test and that of red LED light as control. We found that the blue light irradiation of whisker follicles evoked enhanced unit activities as well as a local field potential in the barrel field of contralateral somatosensory cortex whereas the red light did not. The blue light irradiation also induced blood oxygenation level-dependent (BOLD) and cerebral blood volume (CBV) responses in the barrel field of contralateral somatosensory cortex. It is suggested that the optogenetic whisker stimulation could activate the whisker-barrel cortical pathway of mechanoreceptive signaling. The light-evoked somatosensory would facilitate the study how the complex tactile perception such as form, movement, size and texture is generated. The various and reproducible patterned tactile stimulations could be easily made by the patterned illuminations on the whisker pad without using any mechanical instruments. Since our rat system does not express ChR2 in the nociceptive pathway, it enables one to do in vivo experiments without ethical problems. It would particularly beneficial for the researches using fMRI because the illumination system would not influence the magnetic fields. The light-evoked somatosensory perception should facilitate study of how the complex tactile sense emerges in the brain.
37th Congress of IUPS (Birmingham, UK) (2013) Proc 37th IUPS, SA469
Research Symposium: Optogenetic delivery of touch sense into peripheral and central nervous systems
H. Yawo1,2, T. Honjoh1,2, Z. Ji1,2, Y. Yokoyama1,2, A. Sumiyoshi3, S. Ito1,2, T. Ishizuka1,2, R. Kawashima3, H. Ohta4, Y. Fukazawa5
1. Developmental Biology and Neuroscience, Tohoku University Graduate School of Life Sciences, Sendai, Japan. 2. JST, CREST, Sendai, Japan. 3. Institute of Development, Aging and Cancer, Tohoku University, Sendai, Japan. 4. Department of Physiology, National Defense Medical College, Tokorozawa, Japan. 5. Department of Anatomy and Molecular Cell Biology, Nagoya University Graduate School of Medicine, Nagoya, Japan.
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Where applicable, experiments conform with Society ethical requirements.