The regularity of sustained firing reveals two populations of slowly adapting touch receptors in mouse hairy skin.
Touch is initiated by diverse somatosensory afferents that innervate the skin. The ability to manipulate and classify receptor subtypes is prerequisite for elucidating sensory mechanisms. Merkel cell-neurite complexes, which distinguish shapes and textures, are experimentally tractable mammalian touch receptors that mediate slowly adapting type I (SAI) responses. The assessment of SAI function in mutant mice has been hindered because previous studies did not distinguish SAI responses from slowly adapting type II (SAII) responses, which are thought to arise from different end organs, such as Ruffini endings. Thus we sought methods to discriminate these afferent types. We developed an epidermis-up ex vivo skin-nerve chamber to record action potentials from afferents while imaging Merkel cells in intact receptive fields. Using model-based cluster analysis, we found that two types of slowly adapting receptors were readily distinguished based on the regularity of touch-evoked firing patterns. We identified these clusters as SAI (coefficient of variation = 0.78 +/- 0.09) and SAII responses (0.21 +/- 0.09). The identity of SAI afferents was confirmed by recording from transgenic mice with green fluorescent protein-expressing Merkel cells. SAI receptive fields always contained fluorescent Merkel cells (n = 10), whereas SAII receptive fields lacked these cells (n = 5). Consistent with reports from other vertebrates, mouse SAI and SAII responses arise from afferents exhibiting similar conduction velocities, receptive field sizes, mechanical thresholds, and firing rates. These results demonstrate that mice, like other vertebrates, have two classes of slowly adapting light-touch receptors, identify a simple method to distinguish these populations, and extend the utility of skin-nerve recordings for genetic dissection of touch receptor mechanisms.
Wellnitz
Scott A
SA
Department of Neuroscience, Baylor College of Medicine, Houston, Texas, USA
Lesniak
Daine R
DR
Gerling
Gregory J
GJ
Lumpkin
Ellen A
EA
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D051792:Basic Helix-Loop-Helix Proteins / Q000235:genetics; D049452:Green Fluorescent Proteins / Q000378:metabolism; D006197:Hair; D066298:In Vitro Techniques; D018862:Merkel Cells / Q000145:classification / Q000502:physiology*; D051379:Mice; D008822:Mice, Transgenic; D009412:Nerve Fibers / Q000502:physiology*; D009475:Neurons, Afferent / Q000502:physiology; D010812:Physical Stimulation / Q000379:methods; D012684:Sensory Thresholds / Q000502:physiology; D012867:Skin / Q000294:innervation*; D014110:Touch / Q000502:physiology*
D051792:Basic Helix-Loop-Helix Proteins; D049452:Green Fluorescent Proteins; C500943:Atoh1 protein, mouse; C485184:enhanced green fluorescent protein
J Physiol. 1971 Jan;212(1):21-44
5545179
Nat Protoc. 2009;4(2):174-96
19180088
Eur J Neurosci. 2007 Oct;26(7):1801-12
17897394
J Neurophysiol. 1997 Dec;78(6):2881-8
9405508
Neuron. 2009 Dec 24;64(6):857-70
20064392
J Neurophysiol. 1993 May;69(5):1684-99
8509832
Nature. 2007 Feb 22;445(7130):858-65
17314972
Neuron. 2009 Dec 24;64(6):841-56
20064391
Am J Physiol. 1988 Sep;255(3 Pt 2):F513-9
3414807
Neurosci Lett. 1996 Jul 26;213(1):1-4
8844698
Nat Rev Neurosci. 2009 May;10(5):345-59
19352402
J Neurobiol. 2004 Oct;61(1):30-44
15362151
J Comp Neurol. 1988 Apr 8;270(2):301-12
3379161
Acta Psychol (Amst). 1993 Oct;84(1):41-51
8237455
Exp Brain Res. 1970;10(3):251-64
4985999
J Physiol. 1995 Mar 15;483 ( Pt 3):783-95
7776258
Neurosci Lett. 1986 May 15;66(2):141-6
3725179
J Invest Dermatol. 1993 Jul;101(1 Suppl):75S-81S
8326156
J Neurophysiol. 2002 Apr;87(4):1686-93
11929890
J Neurosci. 2003 May 15;23(10):4054-65
12764092
J Physiol. 1967 Dec;193(3):707-33
16992307
J Neurophysiol. 1981 Dec;46(6):1204-25
7320743
Nat Neurosci. 2009 May;12(5):547-8
19363489
Neuroscience. 2009 Oct 20;163(3):933-41
19596050
J Neurophysiol. 2007 Aug;98(2):668-80
17537905
Nature. 2009 Dec 3;462(7273):651-5
19915548
Gene Expr Patterns. 2003 Aug;3(4):389-95
12915300
Proc Natl Acad Sci U S A. 2004 Oct 5;101(40):14503-8
15448211
Brain Res Brain Res Rev. 2004 Oct;46(2):131-45
15464202
Nature. 2007 Jan 11;445(7124):206-9
17167420
Q J Exp Physiol Cogn Med Sci. 1972 Oct;57(4):417-45
4484588
J Physiol. 1981 Jan;310:117-44
7230030
Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):11845-6
11562504
J Neurophysiol. 1993 Dec;70(6):2411-24
8120590
Clin Chem. 1995 Oct;41(10):1522-5
7586528
J Neurophysiol. 2001 Apr;85(4):1561-74
11287480
J Physiol. 1969 Feb;200(3):763-96
4974746
J Comp Neurol. 2001 Jul 30;436(3):304-23
11438932
Somatosens Res. 1987;5(1):1-17
3685745
Eur J Neurosci. 1999 Nov;11(11):3963-9
10583485
J Physiol. 1973 Dec;235(2):287-315
4763992
J Neurophysiol. 1997 Oct;78(4):1841-50
9325353
J Neurophysiol. 1993 Jul;70(1):397-405
8103089
J Comp Neurol. 2007 Dec 10;505(5):547-61
17924532
J Neurophysiol. 1992 Jan;67(1):125-31
1552314
Brain Res. 1982 Apr 22;238(1):29-43
6282398
J Invest Dermatol. 1977 Jul;69(1):75-82
874346
Science. 2009 Jun 19;324(5934):1580-2
19541997
J Physiol. 2001 Feb 15;531(Pt 1):289-97
11179411
J Neurophysiol. 1968 Nov;31(6):833-48
5710537
Curr Opin Neurobiol. 2001 Aug;11(4):455-61
11502392
J Neurophysiol. 1974 Mar;37(2):267-81
4815205
Physiol Behav. 2002 Dec;77(4-5):589-94
12527004