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Neuropharmacological properties of electrophysiologically identified, visually responsive neurones of the posterior lateral suprasylvian area

A microiontophoretic study

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Summary

Extracellular recordings have been made from 118 electrophysiologically identified neurones lying in the posterior lateral suprasylvian area (PLLS and PLMS) of cats anaesthetized with Nembutal. Eighty-one cells were activated synaptically by the electrical stimulation of cortical and subcortical sites known to be the sources of monosynaptic projections to the lateral suprasylvian area; latencies to such activations have been measured. The locations and sizes of the receptive fields of 55 neurones were determined. The direction sensitivity and ocularity of these cells also were examined.

The effects of various pharmacological agonists and antagonists have been observed on visual responsiveness and synaptic excitability. The excitatory effects of subcortical (dorsal lateral geniculate nucleus and pulvinar nuclear complex) electrical stimulation on the activity of suprasylvian neurones were reduced substantially by the iontophoretic administration of atropine. Antagonists of the receptors for the excitatory amino acids reduced the effectiveness, on the single cell evoked activity, of stimulation of the ipsilateral 17/18 border region and contralateral homotopic lateral suprasylvian area. Both classes of antagonist reduced the magnitude of neuronal responses to photic stimulation, and these response attenuations were additive when the antagonists were ejected concurrently. All of the pharmacological effects were reversible and reproducible. These data lend support to the proposition that acetylcholine and an excitatory amino acid are mediators of synaptic transmission of cortical visual processes in the lateral suprasylvian area.

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References

  1. Baughman RW, Gilbert CD (1980) Aspartate and glutamate as possible neurotransmitters of cells in layer 6 of the visual cortex. Nature 287: 848–850

  2. Bigl V, Schober W (1977) Cholinergic transmission in subcortical and cortical visual centres of rats: No evidence for the involvement of the primary optic system. Exp Brain Res 27: 211–219

  3. Bishop PO, Burke W, Davis R (1962) Single-unit recording from antidromically activated optic radiation neurones. J Physiol (Lond) 162: 432–450

  4. Brown DA, Adams PR (1979) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283: 673–676

  5. Camarda R, Rizzolatti G (1976) Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat. Brain Res 101: 427–443

  6. Collier B, Mitchell JF (1966) The central release of acetylcholine during stimulation of the visual pathway. J Physiol (Lond) 184: 239–254

  7. Collier B, Mitchell JF (1967) The central release of acetylcholine during consciousness and after brain lesions. J Physiol (Lond) 188: 83–98

  8. Crawford JM, Curtis DR (1966) Pharmacological studies on feline Betz cells. J Physiol (Lond) 186: 121–138

  9. Creutzfeldt OD, Guedes RCA, Shoumura K, Watanabe S (1980) Anatomical organization and functional role of afferents to posterior suprasylvian cortex in cats. In: Ádám G, Mészáros I, Bányai EI (eds) Brain and Behaviour, Pergamon Press, Budapest, pp 277–278

  10. Curtis DR (1976) The use of transmitter antagonists in microelectrophoretic investigations of central synaptic transmission. In: Bradley PB, Dhawan BN (eds) Drugs and Central Synaptic Transmission. Macmillan, London, pp 7–35

  11. Dray A, Fox PC, Hilmy M, Somjen GG (1980) The effects of LSD and some analogues on the responses of single cortical neurones of the cat to optical stimulation. Brain Res 200: 105–121

  12. Emson PC, Lindvall O (1979) Distribution of putative neurotransmitters in the neocortex. Neurosci 4: 1–30

  13. Fonnum F, Soreide A, Kvale I, Walker J, Walaas I (1981) Glutamate in cortical fibers. In: DiChara G, Gessa GL (eds) Glutamate as a Neurotransmitter. Raven Press, New York, pp 29–41

  14. Garey LJ, Jones EG, Powell TPS (1968) Interrelationships of striate and extrastriate cortex with primary sites of the visual pathway. J Neurol Neurosurg Psychiatry 31: 135–157

  15. Guedes R, Watanabe S, Creutzfeldt OD (1983) Functional role of association fibres for a visual association area: The posterior suprasylvian sulcus of the cat. Exp Brain Res 49: 13–27

  16. Heath CJ, Jones EG (1971) The anatomical organization of the suprasylvian gyrus of the cat. Ergeb Anat Entwicklungsgesch 45: 1–64

  17. Hebb CO, Krnjević K, Silver A (1963) Effect of undercutting on the acetylcholinesterase and choline acetyltransferase activity in the cat's cerebral cortex. Nature 198: 692

  18. Henry GH, Lund JS, Harvey AR (1978) Cells of the striate cortex projecting to the Clare-Bishop area of the cat. Brain Res 151: 154–158

  19. Hicks TP, Guedes RCA (1981) Synaptic transmission in suprasylvian visual cortex is reduced by excitatory amino acid antagonists. Can J Physiol Pharmacol 59: 893–896

  20. Hicks TP, Guedes RCA, Creutzfeldt OD (1981) Selective synaptic antagonism by atropine and α-aminoadipate of pulvinar and cortical afferents to the suprasylvian visual area (Clare-Bishop area). Brain Res 208: 456–462

  21. Hicks TP, McLennan H (1979) Amino acids and the synaptic pharmacology of granule cells in the dentate gyrus of the rat. Can J Physiol Pharmacol 57: 973–978

  22. Hubel DH, Wiesel TN (1969) Visual area of the lateral suprasylvian gyrus (Clare-Bishop area). J Physiol (Lond) 202: 251–260

  23. Hughes HC (1980) Efferent organization of the cat pulvinar complex, with a note on bilateral claustrocortical and reticulocortical connections. J Comp Neurol 193: 937–963

  24. Hutchinson GB, McLennan H, Wheal HV (1978) The responses of Renshaw cells and spinal interneurones of the rat to L-glutamate and L-aspartate. Brain Res 141: 129–136

  25. Johnson JL (1978) The excitant amino acids glutamic and aspartic acid as transmitter candidates in the vertebrate central nervous system. Prog Neurobiol 10: 155–202

  26. Johnston MV, McKinney M, Coyle JT (1981) Neocortical cholinergic innervation: A description of extrinsic and intrinsic components in the rat. Exp Brain Res 43: 159–172

  27. Kasamatsu T, Pettigrew JD (1979) Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine. J Comp Neurol 185: 139–161

  28. Kasamatsu T, Pettigrew JD, Ary M (1979) Restoration of visual cortical plasticity by local microperfusion of norepinephrine. J Comp Neurol 185: 163–181

  29. Kelly JS (1975) Microiontophoretic application of drugs on to single neurones. In: Iversen LL, Iversen SD, Snyder SH (eds) Handbook of Psychopharmacology, vol 2. Plenum Press, New York, pp 29–68

  30. Kemp JA, Murphy PC, Sillito AM (1981) Cholinergic influences on the response properties of cells in the cat visual cortex. J Physiol (Lond) 320: 16–17

  31. Kennedy H, Baleydier C (1977) Direct projections from thalamic intralaminar nuclei to extrastriate visual cortex in the cat traced with horseradish peroxidase. Exp Brain Res 28: 133–140

  32. Kennedy H, Magnin M (1977) Saccadic influences on single neuron activity in the medial bank of the cat's suprasylvian sulcus (Clare-Bishop area). Exp Brain Res 27: 315–317

  33. Krnjević K, Phillis JW (1963a) Acetylcholine-sensitive cells in the cerebral cortex. J Physiol (Lond) 166: 296–327

  34. Krnjević K, Phillis JW (1963b) Pharmacological properties of acetylcholine-sensitive cells in the cerebral cortex. J Physiol (Lond) 166: 328–350

  35. Krnjević K, Pumain R, Renaud L (1971) The mechanism of excitation in the cerebral cortex. J Physiol (Lond) 215: 247–268

  36. Leventhal AG, Keens J, Törk I (1980) The afferent ganglion cells and cortical projections of the retinal recipient zone (RRZ) of the cat's ‘pulvinar complex’. J Comp Neurol 194: 535–554

  37. Lund Karlsen R (1978) Neurotransmitters of mammalian visual system. In: Fonnum F (ed) Amino Acids as Chemical Transmitters. Plenum Press, New York, pp 241–256

  38. Lund Karlsen R, Fonnum F (1978) Evidence for glutamate as a neurotransmitter in corticofugal fibers to dorsal lateral geniculate body and superior colliculus in rats. Brain Res 151: 457–467

  39. Maciewicz RJ (1974) Afferents to the lateral suprasylvian gyrus of the cat traced with horseradish peroxidase. Brain Res 78: 139–143

  40. Niimi K, Kadota M, Matsushita Y (1974) Cortical projections of the pulvinar nuclear group of the thalamus of the cat. Brain Behav Evol 9: 422–457

  41. Norita M (1977) Demonstration of bilateral claustro-cortical connections in the cat with the method of retrograde axonal transport of horseradish peroxidase. Arch Histol Jpn 40: 1–10

  42. Palmer LA, Rosenquist AC, Tusa RJ (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. J Comp Neurol 177: 237–256

  43. Phillis JW (1976) Acetylcholine and synaptic transmission in the central nervous system. In: Hockman CH, Bieger D (eds) Chemical Transmission in the Mammalian Nervous System. University Park Press, Baltimore, pp 159–213

  44. Raczkowski D, Rosenquist AC (1980) Connections of the parvocellular C laminae of the dorsal lateral geniculate nucleus with the visual cortex in the cat. Brain Res 199: 447–451

  45. Rizzolatti G, Camarda R (1977) Influence of the presentation of remote visual stimuli on visual response properties of cat area 17 and lateral suprasylvian area. Exp Brain Res 19: 107–122

  46. Rosenquist AC, Edwards SB, Palmer LA (1974) An autoradiographic study of the projections of the dorsal lateral geniculate nucleus and the posterior nucleus in the cat. Brain Res 80: 71–93

  47. Shinoda Y, Arnold AP, Asanuma H (1976) Spinal branching of corticospinal axons in the cat. Exp Brain Res 16: 215–234

  48. Shoumura K (1979) The laminar and size distribution of commissural efferent neurons in the cat visual cortex. Arch Histol Jpn 42: 119–128

  49. Shoumura K (1981) Further studies on the size specificity of commissural projecting neurons of layer III in areas 17, 18, 19 and the lateral suprasylvian area of the cat's visual cortex. Arch Histol Jpn 44: 51–69

  50. Shoumura K, Creutzfeldt OD, Guedes RCA, Watanabe S (1981) Thalamic afferents to the banks of the middle suprasylvian sulcus of the cat. Neurosci Lett [Suppl] 6: S19

  51. Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol (Lond) 250: 205–329

  52. Sillito AM (1977) Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex. J Physiol (Lond) 271: 699–720

  53. Sillito AM (1979a) Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol (Lond) 289: 33–53

  54. Sillito AM (1979b) Pharmacological approach to the visual cortex. Trends Neurosci 3: 196–198

  55. Sillito AM (1980) Orientation selectivity and the spatial organization of the afferent input to the striate cortex. Exp Brain Res 41: A9

  56. Spear PD (1979) Behavioral and neurophysiological consequences of visual cortex damage: Mechanisms of recovery. Prog Psychobiol Physiol Psych 8: 45–90

  57. Spear PD, Baumann TP (1975) Receptive-field characteristics of single neurons in the lateral suprasylvian visual area of the cat. J Neurophysiol 38: 1403–1420

  58. Spear PD, Baumann TP (1979) Effects of visual cortex removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. J Neurophysiol 42: 31–56

  59. Spehlmann R, Daniels JC, Smathers CC Jr (1971) Acetylcholine and the synaptic transmission of specific impulses to the visual cortex. Brain 94: 125–138

  60. Stone TW (1972) Cholinergic mechanisms in the rat somatosensory cerebral cortex. J Physiol (Lond) 225: 485–499

  61. Stone TW (1981) Physiological roles for adenosine and adenosine-5′-triphosphate in the nervous system. Neurosci 6: 523–556

  62. Sugiyama M (1979) The projection of the visual cortex on the Clare-Bishop area in the cat. A degeneration study with the electron microscope. Exp Brain Res 36: 433–443

  63. Swadlow HA, Waxman SG (1976) Variations in conduction velocity and excitability following single and multiple impulses of visual callosal axons in the rabbit. Exp Neurol 53: 128–150

  64. Szabadi E (1979) Adrenoceptors on central neurones — microelectrophoretic studies. Neuropharmacology 18: 831–843

  65. Toyama K, Kozasa T (1981) Responses of Clare-Bishop neurones to three dimensional movement of a light stimulus. Vision Res 22: 571–574

  66. Watanabe S, Shoumura K, Iida H, Creutzfeldt OD, Guedes R (1981) Receptive field properties and connection with thalamic nuclei of the posterior lateral suprasylvian cortical neurons. Neurosci Lett [Suppl] 6: S117

  67. Watkins JC (1981) Pharmacology of excitatory amino acid transmitters. In: DeFeudis FV, Mandel P (eds) Amino Acid Neurotransmitters. Raven Press, New York, pp 205–212

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Correspondence to Dr. T. P. Hicks.

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Hicks, T.P., Guedes, R.C.A. Neuropharmacological properties of electrophysiologically identified, visually responsive neurones of the posterior lateral suprasylvian area. Exp Brain Res 49, 157–173 (1983). https://doi.org/10.1007/BF00238576

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Key words

  • Posterior lateral suprasylvian area
  • Receptive fields
  • Synaptic transmission
  • Cholinergic antagonists
  • Amino acid antagonists
  • Cat