Summary
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1.
The responses of pyramidal neurons of rat prepyriform cortex to ionophoretic application of acetylcholine (ACh) were studied in a submerged, perfused brain slice.
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2.
ACh excited some neurons but only if applied to an area near to the cut surface of the slice. This area contained the basal dendrites of the pyramidal cells and some cell bodies. No excitation was seen if ACh was applied at depths of 250µm or more from the cut surface, an area which contained only apical dendrites, although the apical dendrites were very sensitive to excitatory amino acids such as aspartate (Asp) and glutamate (Glu).
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3.
On all neurons which did not discharge to ionophoretic application of ACh, ACh potentiated the response to Glu and Asp. No potentiation of amino acid responses was obtained on apical dendrites. The potentiation had a time course similar to that of the discharge of neurons which fired to ACh. This observation suggests that pyramidal neurons have receptors for ACh on basal but not apical dendrites.
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4.
The ACh response in the basal dendrite-soma region was elicted by pilocarpine and blocked by atropine but not curare. This was true whether the response studied was direct excitation or potentiation of the response to an amino acid.
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5.
The ACh response was associated with a voltage-dependent increase in membrane resistance which had a slow time course and appeared to be due to a turning off of an M current, as described by Brown and Adams (1980) in sympathetic ganglion cells. The effects of ACh were minimal at the resting potential but increased with depolarization. ACh had no effect on the current-voltage relation of the cell, except at depolarized potentials of less than -60 mV.
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6.
Ionophoretic application of Ba2+ to the basal dendritic region resulted in potentiation of the amino acid responses and sometimes induced a discharge similar to that of ACh. Since Ba2+ mimics the ACh response, presumably by a direct blockade of the M channel, the effects of Ba2+ on apical dendrites were tested to determine whether these dendrites contain M channels associated with a transmitter receptor other than ACh. However, Ba2+ did not induce potentiation in apical dendrites, suggesting that M channels are also restricted to the basal dendrites or cell bodies.
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7.
The potentiation of a response to a depolarizing constant-current pulse was comparable in degree and time course to that of amino acid responses, indicating that the ACh potentiation of the amino acid responses is a predictable augmentation of any input which brings the membrane potential into the range of M-channel activation.
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8.
The segregation of ACh receptors to a discrete portion of the cell suggests that they are functional receptors and may be part of a physiologic arrangement which directs different afferent inputs to different portions of the dendritic tree. Such segregation of receptors may also occur on other neurons with distributed inputs.
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References
Adams, P. R., and Brown, D. A. (1980). Luteinizing hormone-releasing factor and muscarinic agonists act on the same voltage-sensitive K+ current in bullfrog sympathetic neurons.Br. J. Pharmacol. 68353–355.
Adams, P. R., Brown, D. A., and Constanti, A. (1982). Pharmacologic inhibition of the M-current.J. Physiol. (Lond.) 332223–262.
Alger, B. E., and Nicoll, R. A. (1982). Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studiedin vitro.J. Physiol. (Lond.) 328125–141.
Andersen, P., Dingledine, R., Gjerstad, L., Langmoen, I. A., and Mosfeldt-Laursen, A. (1980). Two different responses of hippocampal pyramidal cells to application of gamma-amino butyric acid.J. Physiol. (Lond.) 305279–296.
Benardo, L. S., and Prince, D. A. (1982a). Cholinergic excitation of mammalian hippocampal pyramidal cells.Brain Res. 249315–331.
Benardo, L. S., and Prince, D. A. (1982b). Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells.Brain Res. 249333–344.
Bernardi, G., Floris, V., Marciani, M. G., Morocutti, C., and Stanzione, P. (1976). The action of acetylcholine and L-glutamic acid on rat caudate neurons.Brain Res. 114134–138.
Bradley, P. B., and Dray, A. (1976). Observations on the pharmacology of cholinoreceptive neurons in the rat brain stem.Br. J. Pharmacol. 57599–602.
Brown, D. A., and Adams, P. R. (1980). Muscarinic suppression of a novel voltage—sensitive K+ current in a vertebrate neurone.Nature 283673–676.
Brown, D. A., Constanti, A., and Marsh, S. (1980). Angiotensin mimics the action of muscarinic agonists on rat sympathetic neurones.Brain Res. 193614–619.
Carpenter, D. O., and Reese, T. S. (1981). Chemistry and physiology of synaptic transmission. InBasic Neurochemistry, 3rd ed. (G. Siegel, R. Albers, B. Agranoff, and R. Katzman, Eds.), Little, Brown, Boston, pp. 161–168.
Chujo, T., Yamada, Y., and Yamamoto, C. (1975). Sensitivity of Purkinje cell dendrites to glutamic acid.Exp. Brain Res. 23293–300.
Constanti, A., Connor, J. D., Galvan, M., and Nistri, A. (1980). Intracellularly-recorded effects of glutamate and aspartate on neurones in the guinea pig olfactory cortex slice.Brain Res. 195403–420.
Constanti, A., Adams, P. R., and Brown, D. A. (1981). Why do barium ions imitate acetylcholine?Brain Res. 206244–250.
Crawford, A. C., and McBurney, R. N. (1977). The synergistic action of L-glutamate and L-aspartate at crustacean excitatory neuromuscular junctions.J. Physiol. (Lond.) 268697–709.
Dodd, J., Dingledine, R., and Kelly, J. S. (1981). The excitatory action of acetylcholine on hippocampal neurones of the guinea pig and rat maintained in vitro.Brain Res. 207109–127.
Eccles, J. C. (1957).The Physiology of Nerve Cells, Oxford University Press, London.
Engberg, I., Flatman, J. A., and Lambert, J. D. C. (1979). The actions of excitatory amino acids on motoneurons in the feline spinal cord.J. Physiol. (Lond.) 288227–261.
ffrench-Mullen, J., Hori, N., and Carpenter, D. (1981). The effects of acetylcholine (ACh) on neurons in the rat prepyriform cortex slice.Fed. Proc. 40196.
Greene, R. W., and Carpenter, D. O. (1981). Biphasic responses to acetylcholine in mammalian reticulospinal neurons.Cell. Mol. Neurobiol. 1401–405.
Hablitz, J. J. (1982). Conductance changes induced by DL-homocysteic acid and N-methyl-DL-aspartic acid in hippocampal neurons.Brain Res. 247149–153.
Halliwell, J. V., and Adams, P. R. (1982). Voltage-clamp analysis of muscarinic excitation in hippocampal neurons.Brain Res. 25071–92.
Hori, N., Auker, C. R., Braitman, D. J., and Carpenter, D. O. (1982). Pharmacologic sensitivity of amino acid responses and synaptic activation ofin vitro prepyriform neurons.J. Neurophysiol. 481289–1301.
Kelly, J. S., Dodd, J., and Dingledine, R. (1979). Acetylcholine as an excitatory and inhibitory transmitter in the mammalian central nervous system.Prog. Brain Res. 49253–266.
Krnjević, K. (1981). Acetylcholine as modulator of amino-acid mediated synaptic transmission. InThe Role of Peptides and Amino Acids as Neurotransmitters (J. B. Lombardi and A. D. Kenny, Eds.), A. R. Liss, New York, pp 127–141.
Krnjević, K., and Phillis, J. W. (1963a). Acetylcholine sensitive cells in the cerebral cortex.J. Physiol. (Lond.) 166296–327.
Krnjević, K., and Phillis, J. W. (1963b). Pharmacological properties of acetylcholine-sensitive cells in the cerebral cortex.J. Physiol. (Lond.) 166328–350.
Krnjević, K., Pumain, R., and Renaud, L. (1971a). Effects of Ba++ and tetraethylammonium on cortical neurons.J. Physiol. (Lond.) 215223–245.
Krnjević, K., Pumain, R., and Renaud, L. (1971b). The mechanism of excitation by acetylcholine in the cerebral cortex.J. Physiol. (Lond.) 215247–268.
Kuba, K., and Koketsu, K. (1976). Analysis of the slow excitatory postsynaptic potential in bullfrog sympathetic ganglion cells.Jap. J. Physiol. 26651–669.
Mesulam, M. M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents.J. Histochem. Cytochem. 26106–117.
Okamoto, K., and Sakai, Y. (1981). Inhibitory actions of taurocyamine, hypotaurine, taurine and GABA on spike discharges of Purkinje cells, and localization of sensitive sites, in guinea pig cerebellar slices.Brain Res. 206371–386.
Price, J. L. (1973). An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex.J. Comp. Neurol. 15087–108.
Sastry, B. R. (1980). Excitatory post-synaptic potential in the mammalian central nervous system associated with an increase in the membrane resistance.Life Sci. 271403–1407.
Schofield, C. N. (1978). Electrical properties of neurones in the olfactory cortex slicein vitro.J. Physiol. (Lond.) 275523–546.
Segal, M. (1980). The action of serotonin in the rat hippocampal slice preparation.J. Physiol. (Lond.) 303423–439.
Shain, W., and Carpenter, D. O. (1981). Mechanisms of synaptic modulation.Int. Rev. Neurosci. 22205–208.
Shepherd, G. M. (1979).The Synaptic Organization of the Brain, Oxford University Press, New York, pp. 289–307, 310-337.
Shute, C. C. D., and Lewis, P. R. (1967). The ascending cholinergic reticular system: Neocortical, olfactory and subcortical projections.Brain Res. 90497–520.
Sinback, C. N., and Shain, W. (1980). Chemosensitivity of single smooth muscle cells to acetylcholine, noradrenaline and histaminein vitro.J. Cell. Physiol. 10299–112.
Spehlmann, R. (1963). Acetylcholine and prostigmine electrophoresis at visual cortical neurons.J. Neurophysiol. 26127–139.
Weight, F. F., Schulman, J. A., Smith, P. A., and Busis, N. A. (1979). Long-lasting synaptic potential and the modulation of synaptic transmission.Fed. Proc. 382084–2094.
Willis, J. A., Myers, P. R., and Carpenter, D. O. (1977). An ionophoretic module which controls electroosmosis.J. Electrophysiol. Tech. 6817–824.
Woody, C. D., Swartz, B. E., and Gruen, E. (1978). Effects of acetylcholine and cyclic GMP on input resistance of cortical neurons in awake cats.Brain Res. 158373–395.
Yarbrough, G. G. (1978). Studies on neuropharmacology of thyrotropin releasing hormone (TRH) and a new TRH analog.Eur. J. Pharmacol. 4819–24.
Zieglgänsberger, W., and Reiter, C. (1974). A cholinergic mechanism in the spinal cord of cats.Neuropharmacology 13519–527.
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ffrench-Mullen, J.M.H., Hori, N., Nakanishi, H. et al. Asymmetric distribution of acetylcholine receptors and M channels on prepyriform neurons. Cell Mol Neurobiol 3, 163–181 (1983). https://doi.org/10.1007/BF00735280
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DOI: https://doi.org/10.1007/BF00735280