Summary
In cortical area 3b of cats, responses of 76 single neurons to punctate indentations were recorded before and during iontophoretic administration of bicuculline methiodide (BMI), a GABAergic antagonist, at levels that did not affect spontaneous activity. Constant amplitude indentations were applied to selected sites along distalproximal and radial-ulnar axes that intersected the most sensitive area in the receptive field. Profiles of response magnitudes were used to measure receptive field dimensions before and during antagonism of GABAergic inhibition. Blockade of GABAergic transmission caused receptive field dimensions of 48 rapidly-adapting neurons to increase an average 141%, or nearly 2.5 times their original size. Analysis of the spatial distribution of inhibition indicated that in-field inhibition was larger than surround inhibition. During BMI administration, response latency was significantly longer for response elicited from the expanded territory than for responses elicited from within the original receptive field, suggesting that receptive field expansion might be mediated by multisynaptic intracortical connections. The magnitude of receptive field expansion was independent of receptive field size or peripheral location. In a substantial number of neurons, however, BMI produced asymmetric expansions that extended only in the proximal direction. For 9 slowly-adapting neurons, BMI produced measureable increases in receptive field dimensions, but these changes were significantly smaller than the changes in rapidly-adapting neurons.
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References
Alloway KD, Burton H (1985) Submodality and columnar organization of the second somatic sensory area in cats. Exp Brain Res 61: 128–140
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
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
Armstrong-James M, Millar J (1979) Carbon fibre microelectrodes. J Neurosci Meth 1: 279–287.
Batuev AS, Alexandrov AA, Scheynikov NA (1982) Picrotoxin acion on the receptive fields of the cat sensorimotor cortex neurons. J. Neurosci. Res. 7: 49–55
Blomfield S (1974) Arithmetical operations performed by nerve cells. Brain Res 69: 115–124
Brown AG (1981) Organization in the spinal cord. Springer, New York
Calford MB, Tweedale R (1988) Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature 332: 446–448.
Chapin JK (1986) Laminar differences in sizes, shapes, and response profiles of cutaneous receptive fields in the rat SI cortex. Exp Brain Res 62: 549–559
Chapin JK, Lin C-S (1984) Mapping the body representation in the SI cortex of anesthetized and awake rats. J.Comp Neurol 229: 199–213
Costanzo RM, Gardner EP (1980) A quantitative analysis of responses of direction-sensitive neurons in somatosensory cortex of awake monkeys. J Neurophysiol 43: 1319–1341.
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
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
Duncan GH, Dreyer, DA, McKenna TM, Whitsel BL (1982) Dose- and time-dependent effects of ketamine on SI neurons with cutaneous receptive fields. J Neurophysiol 47: 677–699
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
Dykes RW, Lamour Y (1988a) Neurons without demonstrable receptive fields outnumber neurons having receptive fields in samples from the somatosensory cortex of anesthetized or paralyzed cats and rats. Brain Res 440: 133–143
Dykes RW, Lamour Y (1988b) An electrophysiological study of single somato-sensory neurons in rat granular cortex serving the limbs: a laminar analysis. J Neurophysiol 60: 703–724
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
Favorov O, Diamond ME, Whitsel BL (1987) Evidence for a mosaic representation of the body surface in area 3b of the somatic cortex of cat. Proc Natl Acad Sci USA 84: 6606–6610
Florence SL, Wall JT, Garraghty PE, Kaas JH (1988) Distribution of skin afferents in the spinal cord and brain stem after nerve section and regeneration. Soc Neurosci Abstr 18: 475
Gardner EP, Costanzo RM (1980) Neuronal mechanisms underlying direction sensitivity of somatosensory cortical neurons in awake monkeys. J. Neurophysiol 43: 1342–1354
Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3: 1116–1133
Harvey SC (1980) Hypnotics and sedatives. In: Oilman AG, Goodman LS, Gilman A (eds) The pharmacological basis of therapeutics. MacMillan Publishing Co, New York, pp 339–375
Hendry SHC, Houser CR, Jones EG, Vaughn JE (1983) Synaptic organization of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol 12: 639–660
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
Killackey HP (1989) Static and dynamic aspects of cortical somatotopy: a critical evaluation. J. Cognit Neurosci 1: 3–11
Krnjevic L, Schwartz S (1967) The action of gamma-aminobutyric acid on cortical neurones. Exp Brain Res 3: 320–336
Lamour Y, Dutar P, Jobert A, Dykes RW (1988) An iontophoretic study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis of glutamate and acetylchloine effects on receptive field properties. J Neurophysiol 60: 725–750
Landry P, Deschenes M (1981) Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat. J Comp Neurol 199: 345–371
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
Looft FJ (1986) Response of cat cutaneous mechanoreeptors to punctate and grating stimuli. J Neurophysiol 56: 208–220
Martin JH, Spencer WA (1985) Mechanoreceptive submodality channel interactions: single unit analysis of afferent inhibition in the primary somatosensory cortex of the cat. Brain Res 327: 279–288
Martin KAC (1988) From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol 73: 637–702
McCormick DA, Connors BW, Lighthall JW, Prince DA (1985)Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 4: 782–806
Merzenich MM (1987) Dynamic neocortical processes and the origins of higher brain functions. In: Changeux JP, Konishi M (eds) The neural and molecular basis of learning. John Wiley & Sons, pp 337–358
Merzenich MM, Kaas JH, Wall JT, Nelson RJ, Sur M, Felleman DJ (1983a) Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8: 33–55
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
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
Metherate R, Dykes RW (1985) Simultaneous recordings from pairs of cat somatosensory cortical neurons with overlapping peripheral receptive fields. Brain Res 341: 119–129
Mountcastle VB (1957) Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 20: 408–434
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
Mountcastle VB, Talbot WH, Kornhuber HH (1966) The neural transformation of mechanical stimuli delivered to the monkey's hand. In: DeRuck AVS, Knight J (eds) Touch, heat and pain. Little Brown, Boston, pp 325–345
Mountcastle VB, Talbot WH, Sakata H, Hyvärinen J (1969)Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys: neuronal periodicity and frequency discrimination. J Neurophysiol 32: 452–484
Olsen RW (1982) Drug interactions at the GABA receptorionophore complex. Ann. Rev. Pharmacol. Toxicol. 22: 245–277
Peters A, Proskauer CC, Ribak CE (1982) Chandelier cells in rat visual cortex. J Comp Neurol 206: 397–416
Rasmusson DD, Turnbull BG (1983) Immediate effects of digit amputation on SI cortex in the racoon: unmasking of inhibitory fields. Brain Res 288: 368–370
Ray RH, Mallach LE, Kruger L (1985) The response of single guard and down hair mechanoreceptors to moving air-jet stimulation. Brain Res 346: 333–347
Rose D (1977) On the arithmetical operation performed by inhibitory synapses onto the neuronal soma. Exp Brain Res 28: 221–223
Rose D, Blakemore C (1974) Effects of bicuculline on functions of inhibition in visual cortex. Nature 249: 375–377
Sillito AM (1977) Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex. J Physiol 271: 699–720
Snow PJ, Nudo RJ, Rivers W, Jenkins WM, Merzenich MM (1988) Somatotopically inappropriate projections from thalamocortical neurons to the SI cortex of the cat demonstrated by the use of intracortical microstimulation. Somatosen Res 5: 349–372
Sur M, Garraghty PE, Bruce CJ (1985) Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1. Brain Res 342: 391–395
Sur M, Merzenich MM, Kass JH (1980) Magnification, receptive-field area, and “hypercolumn” size in areas 3b and 1 of somatosensory cortex in owl monkeys. J Neurophysiol 44: 295–311
Sur M, Wall JT, Kass 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
Toyama K, Kimura M, Tanaka K (1981a) Cross-correlation analysis of interneuronal connectivity in cat visual cortex. J Neurophysiol 46: 191–201
Toyama K, Kimura M, Tanaka K (1981b) Organization of cat visual cortex as investigated by crosscorrelation technique. J Neurophysiol 46: 202–214
Ts'o DY, Gilbert CD, Wiesel TN (1986) Relationship between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 6: 1160–1170
Tsumoto T, Eckart, W, Creutzfeldt OD (1979) Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp Brain Res 34: 351–363
Wilson PD, Meyers ER, Snow PJ (1987) Changes in spinal circuitry in response to alterations of input: an evaluation of the development and basis of contemporary theories. In: Pubols LM, Sessle BJ (eds) Effects of injury of trigeminal and spinal somatosensory systems. Alan R Liss, New York, pp 227–238
Wilson P, Snow PJ (1987) Reorganization of the receptive fields of spinocervical tract neurons following denervation of a single digit in the cat. J Neurophysiol 57: 803–818
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Alloway, K.D., Rosenthal, P. & Burton, H. Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats. Exp Brain Res 78, 514–532 (1989). https://doi.org/10.1007/BF00230239
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DOI: https://doi.org/10.1007/BF00230239