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Differential effects of GABA and bicuculline on rapidly- and slowly-adapting neurons in primary somatosensory cortex of primates

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In cortical area 3b of monkeys, responses of 71 single neurons to controlled indentations of glabrous skin were recorded before and during iontophoretic application of GABA and bicuculline methiodide (BMI), a GABA receptor antagonist. Constant amplitude indentations were applied to selected sites within the receptive fields of neurons representing the glabrous skin on the digits and palm. Profiles of response magnitudes across stimulation sites were used to quantify receptive field dimensions before and during antagonism of GABAergic inhibition. During administration of BMI, the receptive fields of 26 rapidly-adapting neurons were increased by 3–4 times their original size. Response latencies were substantially longer in the region of expansion than in the original receptive field, suggesting that expansion might be mediated by intracortical connections. The expansion of RFs onto adjacent digits after blockade of GABAergic inhibition suggests that somatotopic reorganization following digit amputations may be subserved by existing excitatory connections. The responses of slowly-adapting neurons were separated into two components, a “dynamic” response corresponding to activity elicited by the initial indenting ramp and a “static” response produced by the sustained indentation. Among 8 slowly-adapting neurons tested with BMI, the receptive fields of the dynamic response component increased to an extent that was similar to the change produced in rapidly-adapting neurons. By contrast, the static response component was rarely altered by BMI. Comparison of the responses to administration of GABA revealed that only 12 of 27 slowly-adapting neurons were inhibited in a dose-dependent manner, whereas 37 of 44 rapidly-adapting neurons exhibited significant reduction of responses in the presence of GABA. Hypotheses are proposed to explain the differential effect of BMI and GABA on slowly- and rapidly-adapting cortical neurons.

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  1. Alloway KD, Burton H (1985) Submodality and columnar organization of the second somatic sensory areas in cats. Exp Brain Res 61:128–140

  2. Alloway KD, Burton H (1986) Bicuculline-induced alterations in neuronal responses to controlled tactile stimuli in the second somatosensory cortex of the cat: a microiontophoretic study. Somatosens Res 3:197–211

  3. Alloway KD, Fabri M, Burton H (1990) Ipsilateral corticocortical connections of SI subdivisions in monkeys. Soc Neurosci Abstr 16:228

  4. Alloway KD, Rosenthal P, Burton H (1989) Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats. Exp Brain Res 78:514–532

  5. Alloway KD, Sinclair RJ, Burton H (1988) Responses of neurons in somatosensory cortical area II of cats to high frequency vibratory stimuli during iontophoresis of a GABA antagonist and glutamate. Somatosens Res 6:109–140

  6. Armstrong-James M, Millar J (1979) Carbon fibre microelectrodes. J Neurosci Meth 1:279–287

  7. Batuev AS, Alexandrov AA, Scheynikov NA (1982) Picrotoxin action on the receptive fields of the cat sensorimotor cortex neurons. J Neurosci Res 7:49–55

  8. Blomfield S (1974) Arithmetical operations performed by nerve cells. Brain Res 69:115–124

  9. Brown AG (1981) Organization in the spinal cord. Springer, New York

  10. Chagnac-Amitai Y, Connors BW (1989a) Horizontal spread of synchronized activity in neocortex, and its control by GABA-mediated inhibition. J Neurophysiol 61:747–758

  11. Chagnac-Amitai Y, Connors BW (1989b) Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. J Neurophysiol 62:1149–1162

  12. Chudler EH, Pretel S, Kenshalo DR (1988) Distribution of GAD-immunoreactive neurons in the first (SI) and second (SII) somatosensory cortex of the monkey. Brain Res 456:57–63

  13. Curtis DR, Felix D (1971) The effect of bicuculline upon synaptic inhibition in the cerebral and cerebellar cortices of the cat. Brain Res 34:301–321

  14. DeFelipe J, Conley M, Jones EG (1986a) Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J Neurosci 6:3749–3766

  15. DeFelipe J, Hendry SHC, Jones EG (1986b) A correlative electron microscopic study of basket cells and large GABAergic neurons in the monkey sensory-motor cortex. Neuroscience 17:991–1009

  16. DeFelipe J, Jones EG (1985) Vertical organization of gammaaminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex. J Neurosci 5:3246–3260

  17. Dreifuss JJ, Kelly JS, Krnjevic K (1969) Cortical inhibition and gamma-aminobutyric acid. Exp Brain Res 9:137–154

  18. Dykes RW, Gabor A (1981) Magnification functions and receptive field sequences for submodality-specific bands in SI cortex of cats. J Comp Neurol 202:597–620

  19. Dykes RW, Landry P, Metherate R, Hicks TP (1984) Functional role of GABA in the cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J Neurophysiol 52:1066–1093

  20. Dykes RW, Rasmusson DD, Hoeltzell PB (1980) Organization of primary somatosensory cortex in the cat. J Neurophysiol 43:1527–1546

  21. Fries W, Zieglänsberger W (1974) A method to discriminate axonal from cell body activity and to analyze “silent cells”. Exp Brain Res 21:441–445

  22. Garraghty PE, Sur M (1990) Morphology of single intracellularly stained axons terminating in area 3b of macaque monkeys. J Comp Neurol 294:583–593

  23. Hendry SHC, Jones EG (1986) Reduction in number of immunostained GABAergic neurons in deprived eye dominance columns of monkey area 17. Nature 320:750–753

  24. Houser CR, Vaughn JE, Hendry SHC, Jones EG, Peters A (1984) GABA neurons in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex. Plenum Press, New York, pp 63–89

  25. Jones EG, Coulter JD, Hendry SHC (1978) Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181:291–348

  26. Killackey HP (1989) Static and dynamic aspects of cortical somatotopy: a critical evaluation. J Cognit Neurosci 1:3–11

  27. Koch C, Poggio T, Torre V (1983) Nonlinear interactions in a dendritic tree: localization, timing and role in information processing. Proc Nat Acad Sci USA 80:2799–2802

  28. Krnjevic L, Phillis JW (1963) Iontophoretic studies of neurones in the mammalian cerebral cortex. J Physiol 165:274–304

  29. Krnjevic K, Reiffenstein RJ, Silver A (1970) Chemical sensitivity of neurons in long-isolated slabs of cerebral cortex. Electroencephalog Clin Neurophysiol 29:269–294

  30. Krnjevic L, Schwartz S (1967) The action of gamma-aminobutyric acid on cortical neurones. Exp Brain Res 3:320–336

  31. 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

  32. MacDonald RL, Barker JL (1979) Enhancement of GABA-mediated postsynaptic inhibition in cultured mammalian spinal cord neurons: a common mode of anticonvulsant action. Brain Res 167:323–336

  33. Merzenich MM, Kaas JH, Wall J, Nelson RJ, Sur M, Felleman D (1983a) Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8:33–55

  34. Merzenich MM, Kaas JH, Wall JT, Sur M, Nelson RJ, Felleman DJ (1983b) Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10:639–665

  35. Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM (1984) Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224:591–605

  36. 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 Hosp 105:201–232

  37. Nelson RJ, Sur M, Felleman DJ, Kaas JH (1980) Representation of the body surface in postcentral parietal cortex of Macaca fascicularis. J Comp Neurol 192:611–643

  38. Nicoll RA, Eccles JC, Oshima T, Rubia F (1975) Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates. Nature 258:625–627

  39. Olsen RW (1982) Drug interactions at the GABA receptorionophore complex. Ann Rev Pharmacol Toxicol 22:245–277

  40. Paul RL, Merzenich MM, Goodman H (1972) Representation of slowly adapting and rapidly adapting cutaneous mechanoreceptors of the hand in Brodmann's areas 3 and 1 of Macaca mulatta. Brain Res 36:229–249

  41. Peters A, Proskauer CC, Ribak CE (1982) Chandelier cells in rat visual cortex. J Comp Neurol 206:397–416

  42. Phillips-Conroy J, Jolly CJ, Nystrom P (1986) Palmar dermatoglyphics as a means of identifying individuals in a baboon population. Int J Primatol 7:435–447

  43. Pons TP, Wall JT, Garraghty PE, Cusick CG, Kaas JH (1987) Consistent features of the representation of the hand in area 3b of macaque monkeys. Somatosen Res 4:309–331

  44. Shanks MF, Pearson RCA, Powell TPS (1978) The intrinsic connections of the primary somatic sensory cortex of the monkey. Proc R Soc Lond B 200:95–101

  45. Sillito AM (1975) The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. J Physiol 250:287–304

  46. Somogyi P, Cowey A, Halasz N, Freund TF (1981) Vertical organization of neurons accumulating [3H]-GABA in visual cortex of rhesus monkey. Nature 294:761–763

  47. Sur M (1980) Receptive fields of neurons in areas 3b and 1 of somatosensory cortex in monkeys. Brain Res 198:465–471

  48. Sur M, Merzenich MM, Kaas JH (1980) Magnification, receptivefield area, and “hypercolumn” size in areas 3b and 1 of somatosensory cortex in owl monkeys. J Neurophysiol 44:295–311

  49. Sur M, Wall JT, Kaas JH (1984) Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys. J Neurophysiol 51:724–744

  50. Warren R, Tremblay N, Dykes RW (1989) Quantitative study of glutamic acid decarboxylase-immunoreactive neurons and cytochrome oxidase activity in normal and partially deafferented rat hindlimb somatosensory cortex. J Comp Neurol 288:583–592

  51. Welker E, Soriano E, Van der Loos H (1989) Plasticity in the barrel cortex of the adult mouse: effects of peripheral deprivation on GAD-immunoreactivity. Exp Brain Res 74:441–452

  52. White EL (1979) Thalamocortical synaptic relations: a review with emphasis on the projection of specific thalamic nuclei on the primary sensory areas of the neocortex. Brain Res Rev 1:275–311

  53. White EL (1986) Termination of thalamic afferents in the cerebral cortex. In: Jones EG, Peters A (eds) Cerebral cortex. Plenum Press, New York, pp 271–289

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Correspondence to H. Burton.

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Alloway, K.D., Burton, H. Differential effects of GABA and bicuculline on rapidly- and slowly-adapting neurons in primary somatosensory cortex of primates. Exp Brain Res 85, 598–610 (1991). https://doi.org/10.1007/BF00231744

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Key words

  • Inhibition
  • Iontophoresis
  • Receptive field
  • Submodality
  • Monkey