Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat

The innervation of the vibrissal follicle sinus complexes (FSCs) in the mystacial pad of the rat was examined by lectin binding histofluorescence with the B subunit of Griffonia simplicifolia (GSA) and by immunofluorescence with a wide variety of antibodies for neuronal related structural proteins, enzymes, and peptides. Only anti‐protein gene product 9.5 labeled all sets of innervation. Several types of mechanoreceptors were distributed to specific different targets by medium to large caliber myelinated axons. All were positive for 200 kDa neurofilament subunit, peripherin, and carbonic anhydrase. Their endings expressed synaptophysin. Labeling for the 160 kDa neurofilament subunit, calbindin, and parvalbumin varied. Anti‐Schwann cell protein S100 was completely co‐extensive with the axons, terminal arbors, and endings of the mechanoreceptor afferents including Merkel innervation. At least 15 different sets of unmyelinated innervation were evident based upon distribution and labeling characteristics. They consisted of four basic types: 1) peptidergic; 2) GSA binding; 3) peptidergic and GSA binding; and 4) nonpeptidergic and GSA negative (peptide‐/GSA‐). Previous studies had not revealed that several major sets of unmyelinated innervation were peptide‐/GSA‐. The unmyelinated innervation had detectable peripherin but not 160 kDa or 200 kDa neurofilament subunits. GSA‐positive axons uniquely lacked anti‐S100 immunoreactivity. The dense circumferentially oriented unmyelinated innervation of the inner conical body contained major sets of peptide‐/GSA‐ and GSA innervation as well as a smaller peptidergic GSA component. A small contingent of sympathetic and possibly parasympathetic innervation was affiliated with microvasculature in the FSCs. This study confirms and refutes some previous hypotheses about biochemical and morphological relationships between peripheral innervation and sensory ganglion cells. J. Comp. Neurol. 385:149–184, 1997. © 1997 Wiley‐Liss, Inc.

[1]  F. Rice,et al.  Overexpression of nerve growth factor in skin causes preferential increases among innervation to specific sensory targets , 1997, The Journal of comparative neurology.

[2]  A. Fagan,et al.  Differential dependency of cutaneous mechanoreceptors on neurotrophins, trk receptors, and P75 LNGFR. , 1997, Developmental biology.

[3]  F. Rice,et al.  Comprehensive immunofluorescence and lectin binding analysis of intervibrissal fur innervation in the mystacial pad of the rat , 1997, The Journal of comparative neurology.

[4]  S. Lawson,et al.  Electrophysiological properties of neurones with CGRP‐like immunoreactivity in rat dorsal root ganglia , 1996, The Journal of comparative neurology.

[5]  D. Zimmer,et al.  The S100 protein family: History, function, and expression , 1995, Brain Research Bulletin.

[6]  B. K. Hartman,et al.  Localization of choline acetyltransferase in rat peripheral sympathetic neurons and its coexistence with nitric oxide synthase and neuropeptides. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[7]  T. Maeda,et al.  Postnatal development of periodontal ruffini endings in rat incisors: An immunoelectron microscopic study using protein gene product 9.5 (PGP 9.5) antibody , 1995, The Journal of comparative neurology.

[8]  C. N. Honda,et al.  Differential distribution of calbindin-D28k and parvalbumin in somatic and visceral sensory neurons , 1995, Neuroscience.

[9]  A. Davies,et al.  Trigeminal sensory neurons require extrinsic signals to switch neurotrophin dependence during the early stages of target field innervation. , 1995, Developmental biology.

[10]  F. Rice,et al.  Innervation of nonmystacial vibrissae in the adult rat , 1995, The Journal of comparative neurology.

[11]  K. Fox,et al.  Effect of vibrissae deprivation on follicle innervation, neuropeptide synthesis in the trigeminal ganglion, and S1 barrel cortex plasticity , 1995, The Journal of comparative neurology.

[12]  T. Hökfelt,et al.  Peripheral axotomy increases the expression of galanin message-associated peptide (GMAP) in dorsal root ganglion cells and alters the effects of intrathecal GMAP on the flexor reflex in the rat , 1995, Neuropeptides.

[13]  T. Hökfelt,et al.  Secretory pathways of neuropeptides in rat lumbar dorsal root ganglion neurons and effects of peripheral axotomy , 1995, The Journal of comparative neurology.

[14]  C. Maggi Tachykinins and calcitonin gene-related peptide (CGRP) as co-transmitters released from peripheral endings of sensory nerves , 1995, Progress in Neurobiology.

[15]  J. Arvidsson,et al.  Innervation of the hard palate in the rat studied by anterograde transport of horseradish peroxidase conjugates , 1995, The Journal of comparative neurology.

[16]  J. Epelbaum,et al.  Developmental patterns of somatostatin-receptors and somatostatin-immunoreactivity during early neurogenesis in the rat , 1994, Neuroscience.

[17]  S. Landis,et al.  The appearance of NPY and VIP in sympathetic neuroblasts and subsequent alterations in their expression , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  T. Hökfelt,et al.  Increased Expression of Galanin in the Rat Superior Cervical Ganglion after Pre- and Postganglionic Nerve Lesions , 1994, Experimental Neurology.

[19]  B. Davis,et al.  Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Vega,et al.  Immunohistochemical localization of calcium-binding proteins in the human cutaneous sensory corpuscles , 1994, Neuroscience Letters.

[21]  B. Droz,et al.  Innervation of Putative Rapidly Adapting Mechanoreceptors by Calbindin‐ and Calretinin‐immunoreactive Primary Sensory Neurons in the Rat , 1994, The European journal of neuroscience.

[22]  T. Hökfelt,et al.  Effect of Peripheral Axotomy on Expression of Neuropeptide Y Receptor mRNA in Rat Lumbar Dorsal Root Ganglia , 1994, The European journal of neuroscience.

[23]  J. Nagy,et al.  Emerging relationships between cytochemical properties and sensory modality transmission in primary sensory neurons , 1993, Brain Research Bulletin.

[24]  F. Rice Structure, vascularization, and innervation of the mystacial pad of the rat as revealed by the lectin griffonia simplicifolia , 1993, The Journal of comparative neurology.

[25]  F. Rice,et al.  The innervation of the mystacial pad of the rat as revealed by PGP 9.5 immunofluorescence , 1993, The Journal of comparative neurology.

[26]  F. Rice,et al.  Sequential differentiation of sensory innervation in the mystacial pad of the ferret , 1993, The Journal of comparative neurology.

[27]  T. Hökfelt,et al.  Coexistence and interaction of neuropeptides with substance P in primary sensory neurons, with special reference to galanin , 1993, Regulatory Peptides.

[28]  Y. Kubota,et al.  Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. , 1993, Journal of neurophysiology.

[29]  F. Rice,et al.  Sensory innervation in the inner conical body of the vibrissal follicle‐sinus complex of the rat , 1993, The Journal of comparative neurology.

[30]  T. Chiba,et al.  Distribution of neuropeptides in rat pterygopalatine ganglion: light and electron microscopic immunohistochemical studies. , 1992, Archives of histology and cytology.

[31]  P. Ernfors,et al.  Cells Expressing mRNA for Neurotrophins and their Receptors During Embryonic Rat Development , 1992, The European journal of neuroscience.

[32]  Huajun He,et al.  Transient expression of somatostatin peptide is a widespread feature of developing sensory and sympathetic neurons in the embryonic rat. , 1992, Journal of Neurobiology.

[33]  A. Davies,et al.  Neurotrophic factors promote the maturation of developing sensory neurons before they become dependent on these factors for survival , 1992, Neuron.

[34]  M. Jacquin,et al.  Parvalbumin and calbindin immunocytochemistry reveal functionally distinct cell groups and vibrissa‐related patterns in the trigeminal brainstem complex of the adult rat , 1992, The Journal of comparative neurology.

[35]  P. Micevych,et al.  The Status of Calcitonin Gene‐Related Peptide as an Effector Peptide , 1992, Annals of the New York Academy of Sciences.

[36]  F. Rice,et al.  The morphology and innervation of facial vibrissae in the tammar wallaby, Macropus eugenii. , 1992, Journal of anatomy.

[37]  T. Hökfelt,et al.  Galanin-mediated control of pain: enhanced role after nerve injury. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[38]  R. Morris,et al.  The distribution of binding by isolectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat , 1992, Neuroscience.

[39]  P. Ciofi,et al.  Early transient expression of somatostatin (SRIF) immunoreactivity in dorsal root ganglia during ontogenesis in the rat , 1992, Brain Research.

[40]  J. Fawcett,et al.  The role of Schwann cells in the regeneration of peripheral nerve axons through muscle basal lamina grafts , 1991, Experimental Neurology.

[41]  H. Gainer,et al.  NF‐L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells , 1991, Journal of neuroscience research.

[42]  S. Lawson,et al.  Neurofilament immunoreactivity in populations of rat primary afferent neurons: A quantitative study of phosphorylated and non-phosphorylated subunits , 1991, Journal of neurocytology.

[43]  D. Zimmer,et al.  Isolation of a rat S100α cDNA and distribution of its mRNA in rat tissues , 1991, Brain Research Bulletin.

[44]  P. J. Waddell,et al.  Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. , 1991, The Journal of physiology.

[45]  T. Hökfelt,et al.  Further studies on galanin-, substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: Effects of dorsal rhizotomies and sciatic nerve lesions , 1991, Experimental Neurology.

[46]  F. Rice,et al.  Sensory innervation of the mystacial pad fur of the ferret , 1991, Neuroscience Letters.

[47]  J. Polak,et al.  Silver Impregnation and Immnunohistochemical Study of Nerves in Lumbar Facet Joint Plical Tissue , 1991, Spine.

[48]  S. Lawson,et al.  Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity , 1990, Neuroscience.

[49]  H. Schaible,et al.  Release, spread and persistence of immunoreactive neurokinin A in the dorsal horn of the cat following noxious cutaneous stimulation. Studies with antibody microprobes , 1990, Neuroscience.

[50]  L. Greene,et al.  Ontogeny of the neuronal intermediate filament protein, peripherin, in the mouse embryo , 1990, Neuroscience.

[51]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

[52]  J. Polak,et al.  Reinnervation and neuropeptides in mouse skin flaps. , 1990, Journal of the autonomic nervous system.

[53]  L. Kruger,et al.  Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers , 1990, Journal of neurocytology.

[54]  J. Polak,et al.  The innervation of human teeth and gingival epithelium as revealed by means of an antiserum for protein gene product 9.5 (PGP 9.5). , 1990, The American journal of anatomy.

[55]  R. Coggeshall,et al.  Percentages of dorsal root axons immunoreactive for galanin are higher than those immunoreactive for calcitonin gene-related peptide in the rat , 1990, Brain Research.

[56]  W. Tetzlaff,et al.  Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  D. Alessi,et al.  S100 is preferentially distributed in myelin-forming Schwann cells , 1990, Journal of neurocytology.

[58]  J. Polak,et al.  Neuronal intermediate filaments in rat dorsal root ganglia: differential distribution of peripherin and neurofilament protein immunoreactivity and effect of capsaicin , 1990, Brain Research.

[59]  L. Belluscio,et al.  Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. , 1990, Science.

[60]  Lawrence Kruger,et al.  Analysis of taste bud innervation based on glycoconjugate and peptide neuronal markers , 1990, The Journal of comparative neurology.

[61]  J. C. Kinnamon,et al.  Synapsin I‐like immunoreactivity in nerve fibers associated with lingual taste buds of the rat , 1990, The Journal of comparative neurology.

[62]  S. Lawson,et al.  Cell type and conduction velocity of rat primary sensory neurons with substance p-like immunoreactivity , 1989, Neuroscience.

[63]  C. Woolf,et al.  Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint , 1989, Neuroscience.

[64]  J. Nagy,et al.  Analysis of parvalbumin and calbindin D28k-immunoreactive neurons in dorsal root ganglia of rat in relation to their cytochrome oxidase and carbonic anhydrase content , 1989, Neuroscience.

[65]  K D Wilkinson,et al.  The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. , 1989, Science.

[66]  J. Nagy,et al.  Parvalbumin is highly colocalized with calbindin D28k and rarely with calcitonin gene-related peptide in dorsal root ganglia neurons of rat , 1989, Brain Research.

[67]  M. Szabolcs,et al.  Carbonic anhydrase activity in the peripheral nervous system of rat: the enzyme as a marker for muscle afferents , 1989, Brain Research.

[68]  R. Zigmond,et al.  Localization of vasoactive intestinal peptide‐ and peptide histidine isoleucine amide‐like immunoreactivities in the rat superior cervical ganglion and its nerve trunks , 1989, The Journal of comparative neurology.

[69]  L. Kruger,et al.  Calcitonin‐gene‐related‐peptide‐immunoreactive innervation of the rat head with emphasis on specialized sensory structures , 1989, The Journal of comparative neurology.

[70]  P. Mantyh,et al.  Peripheral patterns of calcitonin‐gene‐related peptide general somatic sensory innervation: Cutaneous and deep terminations , 1989, The Journal of comparative neurology.

[71]  B. Robertson,et al.  Immunocytochemical evidence for the localization of the GM1 ganglioside in carbonic anhydrase-containing and RT 97-immunoreactive rat primary sensory neurons , 1989, Journal of neurocytology.

[72]  Alun M. Davies The trigeminal system: an advantageous experimental model for studying neuronal development. , 1988, Development.

[73]  S. Brain,et al.  Substance P regulates the vasodilator activity of calcitonin gene-related peptide , 1988, Nature.

[74]  R. Chisholm,et al.  A type III intermediate filament gene is expressed in mature neurons , 1988, Neuron.

[75]  N. Yanaihara,et al.  Presence and coexistence of chromogranin A and multiple neuropeptides in Merkel cells of mammalian oral mucosa , 1988, Neuroscience Letters.

[76]  P. De Camilli,et al.  The synaptic vesicle proteins synapsin I and synaptophysin (protein P38) are concentrated both in efferent and afferent nerve endings of the skeletal muscle , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  J. Lauweryns,et al.  Protein gene product 9.5 expression in the lungs of humans and other mammals. Immunocytochemical detection in neuroepithelial bodies, neuroendocrine cells and nerves , 1988, Neuroscience Letters.

[78]  R. Goldman,et al.  Distribution of a novel 57 kDa intermediate filament (IF) protein in the nervous system , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  T. Hökfelt,et al.  Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy , 1987, Neuroscience Letters.

[80]  J W Griffin,et al.  Neurofilament gene expression: a major determinant of axonal caliber. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[81]  B. Trimmer,et al.  Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[82]  K. Araki,et al.  Tissue distribution of rat S-100α and β subunit mRNAs , 1987 .

[83]  L. Guth,et al.  Distribution of carbonic anhydrase activity in neurons of the rat , 1987, The Journal of comparative neurology.

[84]  H. Takagi,et al.  Calcitonin gene-related peptide promotes mechanical nociception by potentiating release of substance P from the spinal dorsal horn in rats , 1987, Brain Research.

[85]  S. Mense,et al.  Non-myelinated afferent fibres do not originate exclusively from the smallest dorsal root ganglion cells in the cat , 1986, Neuroscience Letters.

[86]  B. Munger,et al.  Successive waves of differentiation of cutaneous afferents in rat mystacial skin , 1986, The Journal of comparative neurology.

[87]  B. Munger,et al.  A comparative light microscopic analysis of the sensory innervation of the mystacial pad. II. The common fur between the vibrissae , 1986, The Journal of comparative neurology.

[88]  P. Camilli,et al.  Presence of synapsin I in afferent and efferent nerve endings of vestibular sensory epithelia , 1986, Brain Research.

[89]  B. Munger,et al.  A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle‐sinus complexes , 1986, The Journal of comparative neurology.

[90]  M. Jacquin,et al.  Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. , 1986, Journal of neurophysiology.

[91]  B. Munger,et al.  Degeneration and regeneration of peripheral nerve in the rat trigeminal system. I. Identification and characterization of the multiple afferent innervation of the mystacial vibrissae , 1986, The Journal of comparative neurology.

[92]  T. Jessell,et al.  Lactoseries carbohydrates specify subsets of dorsal root ganglion neurons projecting to the superficial dorsal horn of rat spinal cord , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  T. Hökfelt,et al.  Multiple tachykinins (neurokinin A, neuropeptide K and substance P) in capsaicin-sensitive sensory neurons in the guinea-pig , 1985, Regulatory Peptides.

[94]  S. Lawson,et al.  Monoclonal antibody 2C5: A marker for a subpopulation of small neurones in rat dorsal root ganglia , 1985, Neuroscience.

[95]  J. Dörfl The innervation of the mystacial region of the white mouse: A topographical study. , 1985, Journal of anatomy.

[96]  T. Hökfelt,et al.  Calcitonin gene-related peptide is a potent inhibitor of substance P degradation. , 1985, European journal of pharmacology.

[97]  P. Emson,et al.  Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P , 1985, Neuroscience.

[98]  J. Price An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulations , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[99]  D. Jacobowitz,et al.  Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat , 1985, Peptides.

[100]  P. Emson,et al.  Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: immunohistochemical analysis , 1985, Brain Research.

[101]  H. Morris,et al.  Calcitonin gene-related peptide is a potent vasodilator , 1985, Nature.

[102]  T. Hökfelt,et al.  Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat , 1984, Neuroscience Letters.

[103]  T. Isobe,et al.  S100a0 (αα) Protein Is Present in Neurons of the Central and Peripheral Nervous System , 1984 .

[104]  J. Garson,et al.  A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones , 1984, The Journal of comparative neurology.

[105]  P. Wall,et al.  Effect of peripheral nerve section and nerve crush on spinal cord neuropeptides in the rat; increased VIP and PHI in the dorsal horn , 1984, Neuroscience.

[106]  L. Terenius,et al.  Comparative immunohistochemical and biochemical analysis of pancreatic polypeptide-like peptides with special reference to presence of neuropeptide Y in central and peripheral neurons , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[107]  T. Hökfelt,et al.  Co-existence of peptide HI (PHI) and VIP in nerves regulating blood flow and bronchial smooth muscle tone in various mammals including man , 1984, Peptides.

[108]  A. Davies,et al.  Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion , 1984, The Journal of comparative neurology.

[109]  M. A. Ariano,et al.  Co-localization of cyclic GMP in superior cervical ganglion with peptide neurotransmitters , 1983, Brain Research.

[110]  A. Dhillon,et al.  PGP 9.5—a new marker for vertebrate neurons and neuroendocrine cells , 1983, Brain Research.

[111]  M. Reinecke,et al.  Immunohistochemical localization of vasoactive intestinal polypeptide (VIP) in Merkel cells of various mammals: evidence for a neuromodulator function of the Merkel cell. , 1983, The Journal of investigative dermatology.

[112]  L. Eng,et al.  Carbonic anhydrase activity in first-order sensory neurons of the rat. , 1983, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[113]  B. Munger,et al.  The sensory innervation of primate facial skin. I. Hairy skin , 1983, Brain Research Reviews.

[114]  J. Foreman,et al.  INTERACTION OF NEUROTENSIN WITH THE SUBSTANCE P RECEPTOR MEDIATING HISTAMINE RELEASE FROM RAT MAST CELLS AND THE FLARE IN HUMAN SKIN , 1982, British journal of pharmacology.

[115]  Bruce Lynn,et al.  Primary afferent units from the hairy skin of the rat hind limb , 1982, Brain Research.

[116]  R. Wollmann,et al.  Distribution of S-100 protein outside the central nervous system , 1982, Brain Research.

[117]  S. Hunt,et al.  Fluoride-resistant acid phosphatase-containing neurones in dorsal root ganglia are separate from those containing substance P or somatostatin , 1982, Neuroscience.

[118]  B. Anderton,et al.  Monoclonal antibodies to mammalian neurofilaments , 1981, Bioscience reports.

[119]  B L Munger,et al.  Sensory nerve endings in rhesus monkey sinus hairs , 1980, The Journal of comparative neurology.

[120]  Ichiro Kanazawa,et al.  Substance P: Depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons , 1979, Brain Research.

[121]  S. Narumi,et al.  STIMULATORY EFFECTS OF SUBSTANCE P ON NEURITE EXTENSION AND CYCLIC AMP LEVELS IN CULTURED NEUROBLASTOMA CELLS , 1978, Journal of neurochemistry.

[122]  B. Munger,et al.  The pilo-ruffini complex: A non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin , 1978, Brain Research.

[123]  T. Yohro Structure of the sinus hair follicle in the big‐clawed shrew, Sorex unguiculatus , 1977, Journal of morphology.

[124]  T. Hökfelt,et al.  Immunohistochemical evidence for separate populations of somatostatin-containing and substance P-containing primary afferent neurons in the rat , 1976, Neuroscience.

[125]  S. Ludwin,et al.  The topographical distribution of S‐100 and GFA proteins in the adult rat brain: An immunohistochemical study using horseradish peroxidase‐labelled antibodies , 1976, The Journal of comparative neurology.

[126]  S. Mughal,et al.  Immunohistochemical localisation of S–100 protein in brain , 1975, Nature.

[127]  R. Dykes Afferent fibers from mystacial vibrissae of cats and seals. , 1975, Journal of neurophysiology.

[128]  A. Iggo,et al.  Functional characteristics of mechanoreceptors in sinus hair follicles of the cat , 1973, The Journal of physiology.

[129]  M. R. Chambers,et al.  The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. , 1972, Quarterly journal of experimental physiology and cognate medical sciences.

[130]  B. Nilsson Effects of Sympathetic Stimulation on Mechanoreceptors of Cat Vibrissae , 1972 .

[131]  A. R. Muir,et al.  The structure and function of a slowly adapting touch corpuscle in hairy skin , 1969, The Journal of physiology.

[132]  A. Iggo,et al.  A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit , 1967, The Journal of physiology.

[133]  B. Munger,et al.  The ultrastructure and innervation of rat vibrissae , 1966, The Journal of comparative neurology.

[134]  W. Montagna,et al.  The tactile hair follicles in the mouse , 1953, The Anatomical record.

[135]  Whei-Min Lin,et al.  Epidermal denervation and its effects on keratinocytes and Langerhans cells , 1996, Journal of neurocytology.

[136]  E. Jones,et al.  The Barrel Cortex of Rodents , 1995, Cerebral Cortex.

[137]  A. Fox,et al.  Chapter 14 Peptidergic afferents: physiological aspects , 1995 .

[138]  S. Lawson Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: substance P, CGRP and somatostatin. , 1995, Progress in brain research.

[139]  F. Rice Comparative Aspects of Barrel Structure and Development , 1995 .

[140]  T. Hökfelt,et al.  The chemical neuroanatomy of sympathetic ganglia. , 1993, Annual review of neuroscience.

[141]  P. Snow,et al.  Plasticity and the Mystacial Vibrissae of Rodents , 1991 .

[142]  D. Simons,et al.  Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. , 1990, Somatosensory & motor research.

[143]  J. Polak,et al.  Peptide-containing nerves in the rat femoral artery and vein. An immunocytochemical and vasomotor study. , 1989, Blood vessels.

[144]  L. Kruger,et al.  Morphological features of thin sensory afferent fibers: a new interpretation of 'nociceptor' function. , 1988, Progress in brain research.

[145]  L. Kruger,et al.  Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated "nociceptor" thin axons in rat testis and cornea whole-mount preparations. , 1988, Somatosensory research.

[146]  L. Kruger,et al.  Acid phosphatase as a selective marker for a class of small sensory ganglion cells in several mammals: spinal cord distribution, histochemical properties, and relation to fluoride-resistant acid phosphatase (FRAP) of rodents. , 1988, Somatosensory research.

[147]  C. Nurse,et al.  Development of Merkel cell populations with contrasting sensitivities to neonatal deafferentation in the rat whisker pad. , 1988, Somatosensory & motor research.

[148]  H. Thoenen,et al.  Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor , 1987, Nature.

[149]  J. M. Gibson,et al.  Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 2. Adaptation and coding of stimulus parameters. , 1983, Somatosensory research.

[150]  F. Gros,et al.  Peripherin, a new member of the intermediate filament protein family. , 1983, Developmental neuroscience.

[151]  J M Gibson,et al.  Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 1. Receptive field properties and threshold distributions. , 1983, Somatosensory research.

[152]  K. Andres,et al.  Morphology of cutaneous receptors. , 1982, Annual review of neuroscience.

[153]  P. R. Burgess,et al.  Cutaneous Mechanoreceptors and Nociceptors , 1973 .

[154]  P J Donovick,et al.  Opossum trigeminal afferents associated with vibrissa and rhinarial mechanoreceptors. , 1973, Brain, behavior and evolution.

[155]  W. Welker,et al.  Coding of somatic sensory input by vibrissae neurons in the rat's trigeminal ganglion. , 1969, Brain research.

[156]  G. Hoggan,et al.  Forked Nerve Endings on Hairs. , 1893, Journal of anatomy and physiology.