Skip to main content

Strategies to Probe Mechanoreception: From Mechanical to Optogenetic Approaches

  • Chapter
Optogenetics

Abstract

There remain many questions about the rules governing the neural representation of touch; how the spatio-temporal patterns of points are integrated in the brain to generate the complex senses such as shape, size, weight, movement, and texture. Conventionally, the touch sense has been artificially generated mechanically or electrically with insufficient spatio-temporal resolution. Recently, the somatosensory system has been optogenetically investigated with the expression of optogenetic molecular reagents (OMRs) such as channelrhodopsin (ChR)-2 and halorhodopsin (NpHR). In a transgenic rat model that expresses ChR2 in peripheral mechanoreceptive neurons in the dorsal root ganglion (DRG) and the trigeminal ganglion (TG), blue light irradiation on skin or whiskers evoked a touch-dependent response in the cortex. Thus, various and reproducible patterned touch stimulations could be made by the patterned irradiations on the skin or whiskers. Optogenetic approaches could open a new avenue to investigate the neural representation of complex touch patterns using a combination of electrophysiological and imaging techniques.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aggestam F, Cahusac PM (2007) Behavioural lateralization of tactile performance in the rat. Physiol Behav 91:335–339

    Article  CAS  PubMed  Google Scholar 

  • Ahissar E, Sosnik R, Haidarliu S (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406:302–306

    Article  CAS  PubMed  Google Scholar 

  • Arabzadeh E, Zorzin E, Diamond ME (2005) Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol 3:e17

    Article  PubMed Central  PubMed  Google Scholar 

  • Arrenberg AB, Del Bene F, Baier H (2009) Optical control of zebrafish behavior with halorhodopsin. Proc Natl Acad Sci U S A 106:17968–17973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Avermann M, Tomm C, Mateo C et al (2012) Microcircuits of excitatory and inhibitory neurons in layer 2/3 of mouse barrel cortex. J Neurophysiol 107:3116–3134

    Article  CAS  PubMed  Google Scholar 

  • Bezdudnaya T, Castro-Alamancos MA (2011) Superior colliculus cells sensitive to active touch and texture during whisking. J Neurosci 106:332–346

    Google Scholar 

  • Björnsdotter M, Löken L, Olausson H et al (2009) Somatotopic organization of gentle touch processing in the posterior insular cortex. J Neurosci 29:9314–9320

    Article  PubMed  Google Scholar 

  • Boada MD, Houle TT, Eisenach JC et al (2010) Differing neurophysiologic mechanosensory input from glabrous and hairy skin in juvenile rats. J Neurophysiol 104:3568–3575

    Article  PubMed Central  PubMed  Google Scholar 

  • Boyden ES, Zhang F, Bamberg E et al (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268

    Article  CAS  PubMed  Google Scholar 

  • Brecht M, Preilowski B, Merzenich MM (1997) Functional architecture of the mystacial vibrissae. Behav Brain Res 84:81–97

    Article  CAS  PubMed  Google Scholar 

  • Celikel T, Sakmann B (2007) Sensory integration across space and in time for decision making in the somatosensory system of rodents. Proc Natl Acad Sci U S A 104:1395–1400

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen LM, Turner GH, Friedman RM et al (2007) High-resolution maps of real and illusory tactile activation in primary somatosensory cortex in individual monkeys with functional magnetic resonance imaging and optical imaging. J Neurosci 27:9181–9191

    Article  CAS  PubMed  Google Scholar 

  • Daou I, Tuttle AH, Longo G et al (2013) Remote optogenetic activation and sensitization of pain pathways in freely moving mice. J Neurosci 33:18631–18640

    Article  CAS  PubMed  Google Scholar 

  • Diamond ME, von Heimendahl M, Knutsen PM et al (2008) ‘Where’ and ‘what’ in the whisker sensorimotor system. Nat Rev Neurosci 9:601–612

    Article  CAS  PubMed  Google Scholar 

  • Douglass AD, Kraves S, Deisseroth K et al (2008) Escape behavior elicited by single, channelrodopsin-2-evoked spikes in zebrafish somatosensory neurons. Curr Biol 18:1133–1137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ego-Stengel V, Mello e Souza T, Jacob V et al (2005) Spatiotemporal characteristics of neuronal sensory integration in the barrel cortex of the rat. J Neurophysiol 93:1450–1467

    Article  PubMed  Google Scholar 

  • Erzurumlu RS, Murakami Y, Rijli FM (2010) Mapping the face in the somatosensory brainstem. Nat Rev Neurosci 11:252–263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Greenspan JD (1992) Influence of velocity and direction of surface-parallel cutaneous stimuli on responses of mechanoreceptors in feline hairy skin. J Neurophysiol 68:876–889

    CAS  PubMed  Google Scholar 

  • Hägglund M, Borgius L, Dougherty KJ et al (2010) Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat Neurosci 13:246–252

    Article  PubMed  Google Scholar 

  • Hentschke H, Haiss F, Schwarz C (2006) Central signal rapidly switch tactile processing in rat barrel cortex during whisker movements. Cereb Cortex 16:1142–1156

    Article  PubMed  Google Scholar 

  • Holtzman T, Rajapaksa T, Mostofi A (2006) Different responses of rat cerebellar purkinje cells and Golgi cells evoked by widespread convergent sensory inputs. J Physiol 574:491–507

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Honjoh T, Ji ZG, Yokoyama Y et al (2014) Optogenetic patterning of whisker-barrel cortical system in transgenic rat expressing channelrhodopsin-2. PLoS One 9:e93706

    Article  PubMed Central  PubMed  Google Scholar 

  • Huber D, Petreanu L, Ghitani N (2008) Sparse optical microstimulation in barrel cortex drives learned behavior in freely moving mice. Nature 451:61–64

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hull C, Adesnik H, Scanziani M (2009) Neocortical disynaptic inhibition requires somatodendritic integration in interneurons. J Neurosci 29:8991–8995

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Husson SJ, Costa WS, Wabnig S et al (2012) Optogenetic analysis of a nociceptor neuron and network reveals ion channels acting downstream of primary sensors. Curr Biol 22:743–752

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ishizuka T, Kakuda M, Araki R et al (2006) Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci Res 54:85–94

    Article  CAS  PubMed  Google Scholar 

  • Iyer SM, Montgomery KL, Towne C et al (2014) Virally mediated optogenetic excitation and inhibition of pain in freely moving nontransgenic mice. Nat Biotechnol 32:274–278

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jacob V, Petreanu L, Wright N et al (2012) Regular spiking and intrinsic bursting pyramidal cells show orthogonal forms of experience-dependent plasticity in layer V of barrel cortex. Neuron 73:391–404

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jennings E, Fitzgerald M (1998) Postnatal changes in responses of rat dorsal horn cells to afferent stimulation: a fibre-induced sensation. J Physiol 509:859–868

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ji ZG, Ito S, Honjoh T et al (2012) Light-evoked somatosensory perception of transgenic rats that express channelrhodopsin-2 in dorsal root ganglion cells. PLoS One 7:e32699

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Knutsen PM, Ahissar E (2009) Orthogonal coding of object location. Trends Neurosci 32:101–109

    Article  CAS  PubMed  Google Scholar 

  • Krupa DJ, Matell MS, Brisben AJ et al (2001) Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci 21:5752–5763

    CAS  PubMed  Google Scholar 

  • Li CX, Callaway JC, Waters RS (2002) Removal of GABAergic inhibition alters subthreshold input in neurons in forepaw barrel subfield (FBS) in rat first somatosensory cortex (SI) after digit stimulation. Exp Brain Res 45:411–428

    Article  Google Scholar 

  • Li X, Gutierrez DV, Hanson MG et al (2005) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc Natl Acad Sci U S A 102:17816–17821

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li W, Kang L, Piggott BJ et al (2011) The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat Commun 2:315

    Google Scholar 

  • Low SE, Ryan J, Sprague SM (2010) Touché is required for touch-evoked generator potentials within vertebrate sensory neurons. J Neurosci 30:9359–9367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maksimovic S, Nakatani M, Baba Y et al (2014) Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 29:617–621. doi:10.1038/nature13250

  • Mateo C, Avermann M, Gentet LJ et al (2011) In vivo optogenetic stimulation of neocortical excitatory neurons drives brain-state-dependent inhibition. Curr Biol 21:1593–1602

    Article  CAS  PubMed  Google Scholar 

  • Mirabella G, Battiston S, Diamond ME (2001) Integration of multiple-whisker inputs in rat somatosensory cortex. Cereb Cortex 11:164–170

    Article  CAS  PubMed  Google Scholar 

  • Morissette J, Bower JM (1996) Contribution of somatosensory cortex to responses in the rat cerebellar granule cell layer following peripheral tactile stimulation. Exp Brain Res 109:240–250

    Article  CAS  PubMed  Google Scholar 

  • Morita T, Kang H, Wolfe J et al (2011) Psychometric curve and behavioral strategies for whisker-based texture discrimination in rats. PLoS One 6:e20437

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Müller J (1834–1840) Handbuch der Physiologie des Menschen für Vortesungen. J. Holscher, Coblenz, Translated section (Elements of Physiology, Book V. Of The Senses) in Rand B (1912) The classical psychologists. Houghton Mifflin, Boston

    Google Scholar 

  • Nagel G, Szellas T, Huhn W et al (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100:13940–13945

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nicholls JG, Martin AR, Wallace BG et al (2001) From neuron to brain, 4th edn. Sinauer associates Inc, Sunderland

    Google Scholar 

  • O’Connor DH, Huber D, Svoboda K (2009) Reverse engineering the mouse brain. Nature 461:923–929

    Article  PubMed  Google Scholar 

  • O’Connor DH, Clack NG, Huber D et al (2010) Vibrissa-based object localization in head-fixed mice. J Neurosci 30:1947–1967

    Article  PubMed  Google Scholar 

  • Petersen CC (2007) The functional organization of the barrel cortex. Neuron 56:339–355

    Article  CAS  PubMed  Google Scholar 

  • Petreanu L, Huber D, Sobczyk A (2007) Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci 10:663–668

    Article  CAS  PubMed  Google Scholar 

  • Pidoux M, Mahon S, Deniau JM et al (2011) Integration and propagation of somatosensory responses in the corticostriatal pathway: an intracellular study in vivo. J Physiol 589:263–281

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ramirez A, Pnevmatikakis EA, Merel J et al (2014) Spatiotemporal receptive fields of barrel cortex revealed by reverse correlation of synaptic input. Nat Neurosci 17:866–875

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reed JL, Pouget P, Qi HX et al (2008) Widespread spatial integration in primary somatosensory cortex. Proc Natl Acad Sci U S A 105:10233–10237

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ritt JT, Andermann ML, Moore CI (2008) Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats. Neuron 57:599–613

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rowland NC, Jaeqer D (2005) Coding of tactile responses properties in the rat deep cerebellar nuclei. J Neurophysiol 94:1236–1251

    Article  PubMed  Google Scholar 

  • Saito K, Hitomi S, Suzuki I et al (2008) Modulation of trigeminal spinal subnucleus caudalis neuronal activity following regeneration of transected inferior alveolar nerve in rats. J Neurophysiol 99:2251–2263

    Article  PubMed  Google Scholar 

  • Simons DJ (1985) Temporal and spatial integration in the rat SI vibrissa cortex. J Neurophysiol 54:615–635

    CAS  PubMed  Google Scholar 

  • Tomita H, Sugano E, Fukazawa Y et al (2009) Visual properties of transgenic rats harboring the channelrhodopsin-2 gene regulated by the thy-1.2 promoter. PLoS One 4:e7679

    Google Scholar 

  • Tremblay N, Bushnell MC, Duncan GH (1993) Thalamic VPM nucleus in the behaving monkey. II. Response to air-puff stimulation during discrimination and attention tasks. J Neurophysiol 69:753–763

    CAS  PubMed  Google Scholar 

  • Umeda K, Shoji W, Sakai S et al (2013) Targeted expression of a chimeric channelrhodopsin in zebrafish under regulation of Gal4-UAS system. Neurosci Res 75:69–75

    Article  CAS  PubMed  Google Scholar 

  • Van Camp N, Verhoye M, Van der Linden A (2006) Stimulation of the rat somatosensory cortex at different frequencies and pulse widths. NMR Biome 19:10–17

    Article  Google Scholar 

  • Wang H, Zylka MJ (2009) Mrgprd-expressing polymodal nociceptive neurons innervate most known classes of substantia gelatinosa neurons. J Neurosci 29:13202–13209

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Warren S, Kelahan AM, Pubols BH Jr (1986) The somatosensory thalamus of the raccoon: properties of single neurons responsive to light mechanical stimulation of the forepaw. J Neurosci 6:308–317

    CAS  PubMed  Google Scholar 

  • Yawo H, Asano T, Sakai S et al (2013) Optogenetic manipulation of neural and non-neural functions. Dev Growth Differ 55:474–490

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhi-Gang Ji .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Ji, ZG., Ishizuka, T., Yawo, H. (2015). Strategies to Probe Mechanoreception: From Mechanical to Optogenetic Approaches. In: Yawo, H., Kandori, H., Koizumi, A. (eds) Optogenetics. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55516-2_21

Download citation

Publish with us

Policies and ethics