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Interactions between inputs from adjacent digits in somatosensory thalamus and cortex of the raccoon

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Abstract

Interactions between somatosensory afferents arriving from different points in the periphery play an important role in sensory discrimination and also provide the substrate for plasticity following peripheral injury. To examine the extent and time course of such interactions, extracellular recordings were made from neurons in the primary somatosensory cortex and the ventroposterior lateral thalamus of anesthetized raccoons. Interactions between adjacent digits were studied using the conditioning-test paradigm in which a test pulse was delivered to the digit containing the neuron's receptive field (the on-focus digit) at various intervals following conditioning stimulation of an adjacent, off-focus digit. Off-focus stimulation produced predominantly inhibition of the test response with a maximum effect at 20–40 ms in both cortex and thalamus. The mean inhibition was approximately twice as large in the thalamus as in the cortex. Recordings were made in other animals after unmyelinated C fibers had been destroyed in the on-focus digit by subcutaneous injection of capsaicin. This resulted in a doubling of the responses evoked by the test stimulus in both regions, but the spontaneous discharge rate was not changed. The amount of inhibition produced in the cortex was unchanged by capsaicin treatment, but was reduced in the thalamus compared to control animals. This indicates that capsaicin-sensitive peripheral afferents provide a tonic control over interdigit inhibition in the thalamus.

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References

  • Andersen P, Brooks CM, Eccles JC, Sears TA (1964a) The ventro-basal nucleus of the thalamus: potential fields, synaptic transmission and excitability of both presynaptic and post-synaptic components. J Physiol Lond 174:348–369

    CAS  Google Scholar 

  • Andersen P, Eccles JC, Sears TA (1964b) The ventro-basal complex of the thalamus: types of cells, their responses and their functional organization. J Physiol 174:370–399

    CAS  Google Scholar 

  • Burton H, Craig AD (1983) Spinothalamic projections in cat, raccoon and monkey: a study based on anterograde transport of horseradish peroxidase. In: Macchi G, Rustioni A, Spreafico R (eds) Somatosensory integration in the thalamus. Elsevier, Amsterdam, pp 17–41

  • Calford MB (2002) Dynamic representational plasticity in sensory cortex. Neuroscience 111:709–738

    Article  CAS  PubMed  Google Scholar 

  • Calford MB, Tweedale R (1990) The capacity for reorganization in adult somatosensory cortex. In: Rowe M, Aitkin L (eds) Information processing in mammalian auditory and tactile systems. Liss, New York, pp 221–236

  • Calford MB, Tweedale R (1991a) Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox. J Neurophysiol 65:178–187

    CAS  PubMed  Google Scholar 

  • Calford MB, Tweedale R (1991b) C-fibres provide a source of masking inhibition to primary somatosensory cortex. Proc R Soc. Lond B Biol Sci 243:269–275

    CAS  Google Scholar 

  • Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824

    CAS  PubMed  Google Scholar 

  • Chowdhury SA, Rasmusson DD (2003) Corticocortical inhibition of peripheral inputs within primary somatosensory cortex: the role of GABAA and GABAB receptors. J Neurophysiol (in press)

    Google Scholar 

  • Dick SH, Rasmusson DD (2002) Effects of temporary deafferentation on raccoon postsynaptic dorsal column neurons. Brain Res 950:239–244

    Article  CAS  PubMed  Google Scholar 

  • Doetsch GS, Norelle A, Mark EK, Standage GP, Lu SM, Lin RCS (1993) Immunoreactivity for GAD and three peptides in somatosensory cortex and thalamus of the raccoon. Brain Res Bull 31:553–563

    Article  CAS  PubMed  Google Scholar 

  • Emri Z, Turner JP, Crunelli V (1996) Tonic activation of presynaptic GABAB receptors on thalamic sensory afferents. Neuroscience 72:689–698

    Article  CAS  PubMed  Google Scholar 

  • Gardner EP, Costanzo RM (1980) Temporal integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. J Neurophysiol 43:444–468

    CAS  PubMed  Google Scholar 

  • Haimann C, Margnelli M, Sotgiu ML (1978) Variability of peripheral representation in ventrobasal thalamic nuclei of the cat: effects of chloralose treatment. Exp Neurol 69:469–483

    Google Scholar 

  • Harding GW, Stogsdill RM, Towe AL (1979) Relative effects of pentobarbital and chloralose on the responsiveness of neurons in sensorimotor cerebral cortex of the domestic cat. Neuroscience 4:369–378

    Article  CAS  PubMed  Google Scholar 

  • Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200:341–354

    Article  CAS  PubMed  Google Scholar 

  • Jänig W, Spencer WA, Younkin SG (1979) Spatial and temporal features of afferent inhibition of thalamocortical relay cells. J Neurophysiol 42:1450–1460

    PubMed  Google Scholar 

  • Johnson JI, Welker WI, Pubols BH (1968) Somatotopic organization of raccoon dorsal column nuclei. J Comp Neurol 132:1–44

    PubMed  Google Scholar 

  • Kelahan AM, Doetsch GS (1984) Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens Res 2:49–81

    CAS  PubMed  Google Scholar 

  • Kim U, Ebner FF (1999) Barrels and septa: separate circuits in rat barrel field cortex. J Comp Neurol 408:489–505

    Article  CAS  PubMed  Google Scholar 

  • Koralek K-A, Jensen KF, Killackey HP (1988) Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex. Brain Res 463:346–351

    Article  CAS  PubMed  Google Scholar 

  • Laskin SE, Spencer WA (1979) Cutaneous masking. II. Geometry of excitatory and inhibitory receptive fields of single units in somatosensory cortex of the cat. J Neurophysiol 42:1061–1082

    CAS  PubMed  Google Scholar 

  • Lee SM, Friedberg MH, Ebner FF (1994) The role of GABA-mediated inhibition in the rat ventral posterior medial thalamus. II. Differential effects of GABAA and GABAB receptor antagonists on responses of VPM neurons. J Neurophysiol 71:1716–1726

    CAS  PubMed  Google Scholar 

  • Mountcastle VB, Powell TPS (1959) Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. Bull Johns Hopkins Hospital 105:201–232

    CAS  Google Scholar 

  • Nussbaumer J-C, Loos H van der (1985) An electrophysiological and anatomical study of projections to the mouse cortical barrelfield and its surroundings. J Neurophysiol 53:686–698

    CAS  PubMed  Google Scholar 

  • Nussbaumer J-C, Wall PD (1985) Expansion of receptive fields in the mouse cortical barrelfield after administration of capsaicin to neonates or local application on the infraorbital nerve in adults. Brain Res 360:1–9

    Article  CAS  PubMed  Google Scholar 

  • Petsche U, Fleischer E, Lembeck F, Handwerker HO (1983) The effect of capsaicin application to a peripheral nerve on impulse conduction in functionally identified afferent nerve fibres. Brain Res 265:233–240

    Article  CAS  PubMed  Google Scholar 

  • Pettit MJ, Schwark HD (1996) Capsaicin-induced rapid receptive field reorganization in cuneate neurons. J Neurophysiol 75:1117–1125

    CAS  PubMed  Google Scholar 

  • Pini A, Baranowski R, Lynn B (1990) Long-term reduction in the number of C-fibre nociceptors following capsaicin treatment of a cutaneous nerve in adult rats. Eur J Neurosci 2:89–97

    PubMed  Google Scholar 

  • Rasmusson DD (1982) Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J Comp Neurol 205:313–326

    CAS  PubMed  Google Scholar 

  • Rasmusson DD (1996a) Changes in the organization of the ventroposterior lateral thalamic nucleus after digit removal in adult raccoon. J Comp Neurol 364:92–103

    CAS  PubMed  Google Scholar 

  • Rasmusson DD (1996b) Changes in the response properties of neurons in the ventroposterior lateral thalamic nucleus of the raccoon after peripheral deafferentation. J Neurophysiol 75:2441–2450

    CAS  PubMed  Google Scholar 

  • Rasmusson DD, Northgrave SA (1997) Reorganization of the raccoon cuneate nucleus after peripheral denervation. J Neurophysiol 78:2924–2936

    CAS  PubMed  Google Scholar 

  • Rasmusson DD, Turnbull BG (1983) Immediate effects of digit amputation on S1 cortex in the raccoon: unmasking of inhibitory sites. Brain Res 288:368–370

    CAS  PubMed  Google Scholar 

  • Rasmusson DD, Webster HH, Dykes RW (1992) Neuronal response properties within subregions of raccoon somatosensory cortex one week after digit amputation. Somatosens Motor Res 9:279–289

    CAS  Google Scholar 

  • Rasmusson DD, Louw D, Northgrave SA (1993) The immediate effects of peripheral denervation on inhibitory mechanisms in the somatosensory thalamus. Somatosens Motor Res 10:69–80

    CAS  Google Scholar 

  • Roberts WA, Eaton SA, Salt TE (1992) Widely distributed GABA-mediated afferent inhibition processes within the ventrobasal thalamus of rat and their possible relevance to pathological pain states and somatotopic plasticity. Exp Brain Res 89:363–372

    CAS  PubMed  Google Scholar 

  • Salt TE (1989) Gamma-aminobutyric acid and afferent inhibition in the cat and rat ventrobasal thalamus. Neuroscience 28:17–26

    Article  CAS  PubMed  Google Scholar 

  • Simons DJ (1985) Temporal and spatial integration in the rat S1 vibrissa cortex. J Neurophysiol 54:615–635

    CAS  PubMed  Google Scholar 

  • Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61:311–330

    CAS  PubMed  Google Scholar 

  • Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679–685

    CAS  PubMed  Google Scholar 

  • Turnbull BG, Rasmusson DD (1986) Sensory innervation of the raccoon forepaw. 1. Receptor types in glabrous and hairy skin and deep tissue. Somatosens Res 4:43–62

    PubMed  Google Scholar 

  • Turnbull BG, Rasmusson DD (1990) Acute effects of total or partial digit denervation on raccoon somatosensory cortex. Somatosens Motor Res 7:365–389

    CAS  Google Scholar 

  • Varga C, Sik A, Lavallée P, Deschênes M (2002) Dendroarchitecture of relay cells in thalamic barreloids: a substrate for cross-whisker modulation. J Neurosci 22:6186–6194

    CAS  PubMed  Google Scholar 

  • Waldmeier PC, Wicki P, Feldtrauer JJ, Mickel SJ, Bittiger H, Baumann PA (1994) GABA and glutamate release affected by GABAB receptor antagonists with similar potency: no evidence for pharmacologically different presynaptic receptors. Br J Pharmacol 113:1515–1521

    CAS  PubMed  Google Scholar 

  • Wall PD, Fitzgerald M, Woolf CJ (1982) Effects of capsaicin on receptive fields and on inhibitions in rat spinal cord. Exp Neurol 78:425–436

    CAS  PubMed  Google Scholar 

  • Welker WI, Johnson JI (1965) Correlation between nuclear morphology and somatotopic organization in ventro-basal complex of the raccoon's thalamus. J Anat 99:761–790

    CAS  PubMed  Google Scholar 

  • Welker WI, Seidenstein S (1959) Somatic sensory representation in the cerebral cortex of the raccoon (Procyon lotor). J Comp Neurol 111:469–501

    CAS  Google Scholar 

  • Willis WD, Coggeshall RE (1991) Sensory mechanisms of the spinal cord. Plenum, New York

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Acknowledgements

This work was supported by the Canadian Institutes of Health Research (CIHR) grant MT-06673.

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  1. Departments of Physiology and Biophysics, Dalhousie University, Halifax, Nova Scotia, B3H 4H7, Canada

    K. A. Greek, S. A. Chowdhury & D. D. Rasmusson

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  1. K. A. Greek
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  2. S. A. Chowdhury
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  3. D. D. Rasmusson
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Correspondence to D. D. Rasmusson.

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Greek, K.A., Chowdhury, S.A. & Rasmusson, D.D. Interactions between inputs from adjacent digits in somatosensory thalamus and cortex of the raccoon. Exp Brain Res 151, 364–371 (2003). https://doi.org/10.1007/s00221-003-1493-6

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