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Structures mediating cholinergic reticular facilitation of cortical responses in the cat: effects of lesions in immunocytochemically characterized projections

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Abstract

Cholinergic afferents to the neocortex controlled by the mesencephalic reticular formation (MRF) are known to transiently facilitate cortical excitability. In an attempt to identify the pathway mediating this effect in the cat visual cortex we combined retrograde tracing techniques with immunocytochemical methods to visualize the acetylcholine-synthesizing enzyme choline acetyltransferase (ChAT). In addition we examined, in acute electrophysiological experiments, whether local neurotoxin injections into nuclei of the basal forebrain interfered with the reticular facilitation of cortical evoked potentials. Cholinergic projections to area 17 originate from different centers in the homolateral substantia innominata/internal capsule, the septal nuclei, and the nuclei of the diagonal band of Broca. No direct cholinergic projection from the MRF to the visual cortex was observed. Retrogradely labelled cells intermingled with ChAT-positive neurons in the brainstem generally revealed immunopositivity for catecholaminergic markers. Local injections of neurotoxins in the substantia innominata blocked reticular facilitation, whereas local lesions of the septal nuclei and the nuclei of the diagonal band had no effect on MRF-induced facilitation. The blockage of the reticular facilitation of cortical evoked responses after unilateral lesions of the substantia innominata was bilateral, suggesting a cooperative interaction between basal forebrain structures of the two hemispheres. The anatomical and physiological data are discussed with respect to possible mechanisms of transient brainstem influences on cortical excitability.

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References

  • Bear MF, Singer W (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320:172–176

    Article  CAS  PubMed  Google Scholar 

  • Bear MF, Carnes KM, Ebner FF (1985) An investigation of cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry. J Comp Neurol 234:411–430

    Article  CAS  PubMed  Google Scholar 

  • Bentivoglio M, Macchi G, Rossini P, Tempesta E (1978) Brain stem neurons projecting to neocortex: an HRP study in the cat. Exp Brain Res 31:489–498

    Article  CAS  PubMed  Google Scholar 

  • Boylan MK, Fisher RS, Hull CD, Buchwald NA, Levine MS (1986) Axonal branching of basal forebrain projections to the neocortex: a double-labeling study in the cat. Brain Res 375:176–181

    Article  CAS  PubMed  Google Scholar 

  • Buzsáki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 8:4007–4026

    PubMed  Google Scholar 

  • Divac I (1975) Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res 93:385–398

    Article  CAS  PubMed  Google Scholar 

  • Edwards SB, Olmos JS de (1976) Autoradiographic studies of the projections of the midbrain reticular formation: ascending projections of nucleus cuniformis. J Comp Neurol 165:417–432

    Article  CAS  PubMed  Google Scholar 

  • Fisher RS, Buchwald NA, Hull CD, Levine MS (1988) GABAergic basal forebrain neurons project to the neocortex: the localization of glutamic acid decarboxylase and choline acetyltransferase in feline corticopetal neurons. J Comp Neurol 272:489–502

    Article  CAS  PubMed  Google Scholar 

  • Francesconi W, Müller CM, Singer W (1988) Cholinergic mechanisms in the reticular control of transmission in the cat lateral geniculate nucleus. J Neurophysiol 59:1690–1718

    CAS  PubMed  Google Scholar 

  • Henderson Z (1987) Source of cholinergic input to ferret visual cortex. Brain Res 412:261–268

    Article  CAS  PubMed  Google Scholar 

  • Johnston MV, Young AC, Coyle, JT (1981) Laminar distribution of cholinergic markers in neocortex: effects of lesions. J Neurosci Res 6:597–607

    Article  CAS  PubMed  Google Scholar 

  • Jones BE, Beaudet A (1987a) Retrograde labeling of neurons in the brainstem following injections of [3H]choline into the forebrain of the rat. Exp Brain Res 65:437–448

    CAS  PubMed  Google Scholar 

  • Jones BE, Beaudet A (1987b) Distribution of acetylcholine and catecholamine neurons in the cat brainstem: a choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J Comp Neurol 261:15–32

    Article  CAS  PubMed  Google Scholar 

  • Katz LC, Burkhalter A, Dreyer WJ (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498–500

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Lamour Y, Dutar P, Jobert A (1984) Cortical projections of the nucleus of the diagonal band of Broca and of the substantia innominata in the rat: an anatomical study using the anterograde transport of a conjugate of wheat germ agglutinin and horseradish peroxidase. Neuroscience 12:395–408

    Article  CAS  PubMed  Google Scholar 

  • Lewandowski M, Müller CM, Singer W (1993) Reticular facilitation of cat visual cortical responses is mediated by nicotinic and muscarinic cholinergic mechanisms. Exp Brain Res 96:1–7

    CAS  PubMed  Google Scholar 

  • Lima AD de, Singer W (1987) The brainstem projection to the lateral geniculate nucleus in the cat: identification of cholinergic and monoaminergic elements. J Comp Neurol 259:92–121

    Article  PubMed  Google Scholar 

  • McCormick DA, Prince DA (1986) Mechanisms of action of acetylcholine in the guinea pig cerebral cortex, in vitro. J Physiol (Lond) 375:169–194

    CAS  Google Scholar 

  • McDonald JW, Silverstein FS, Johnston MV (1988) Neurotoxicity of N-methyl-d-aspartate is markedly enhanced in developing rat central nervous system. Brain Res 459:200–203

    Article  CAS  PubMed  Google Scholar 

  • Metherate R, Weinberger NM (1989) Acetylcholine produces stimulus specific receptive-field alterations in cat auditory cortex. Brain Res 480:372–377

    Article  CAS  PubMed  Google Scholar 

  • Metherate R, Tremblay N, Dykes RW (1987) Acetylcholine permits long-term enhancement of neuronal responsiveness in cat primary somatosensory cortex. Neuroscience 1:75–81

    Article  Google Scholar 

  • Mitchell SJ, Richardson RT, Baker FH, De Long MR (1987) The primate nucleus basalis of Meynert: neuronal activity related to a visuomotor tracking task. Exp Brain Res 68:506–515

    CAS  PubMed  Google Scholar 

  • Moruzzi G, Magoun HW (1949) Brainstem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455–473

    Article  CAS  PubMed  Google Scholar 

  • Müller CM, Singer W (1989) Acetylcholine-induced inhibition in the cat visual cortex is mediated by a GABAergic mechanism. Brain Res 487:335–342

    Article  PubMed  Google Scholar 

  • Nistri A, Bartolini A, Deffenu G, Pepeu G (1972) Investigations into the release of acetylcholine from the cerebral cortex of the cat: effects of amphetamine, of scopolamine and of septal lesions. Neuropharmacology 11:665–674

    Article  CAS  PubMed  Google Scholar 

  • Pearson RCA, Neal JW, Powell TPS (1986) Hypertrophy of cholinergic neurones of the basal nucleus in the rat following damage of the contralateral nucleus. Brain Res 382:149–152

    Article  CAS  PubMed  Google Scholar 

  • Price JL, Stern R (1983) Individual cells in the nucleus basalis-diagonal band complex have restricted axonal projections to the cerebral cortex in the rat. Brain Res 269:352–356

    Article  CAS  PubMed  Google Scholar 

  • Prusky GT, Shaw C, Cynader MS (1988) The distribution and ontogenesis of [3H]nicotine binding sites in cat visual cortex. Brain Res Dev Brain Res 39:161–176

    Article  CAS  Google Scholar 

  • Richardson RT, De Long MR (1986) Nucleus basalis of Meynert neuronal activity during a delayed response task in monkey. Brain Res 399:364–368

    Article  CAS  PubMed  Google Scholar 

  • Sato H, Hata Y, Hagihara K, Tsumoto T (1987a) Effects of cholinergic depletion on neuron activities in the cat visual cortex. J Neurophysiol 58:781–794

    CAS  PubMed  Google Scholar 

  • Sato H, Hata Y, Masui H, Tsumoto T (1987b) A functional role of cholinergic innervation to neurons in the cat visual cortex. J Neurophysiol 58:765–780

    CAS  PubMed  Google Scholar 

  • Semba K, Reiner PB, McGeer EG, Fibinger HC (1988a) Noncholinergic basal forebrain neurons project to the contralateral basal forebrain in the rat. Neurosci Lett 84:23–28

    Article  CAS  PubMed  Google Scholar 

  • Semba K, Reiner PB, McGeer EG, Fibinger HC (1988b) Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 267:433–453

    Article  CAS  PubMed  Google Scholar 

  • Shaw C, Needler MC, Cynader M (1984) Ontogenesis of muscarinic acetylcholine binding sites in cat visual cortex: reversal of specific laminar distribution during the critical period. Brain Res Dev Brain Res 14:295–299

    Article  CAS  Google Scholar 

  • Sillito AM, Kemp JA (1983) Cholinergic modulation of the functional organization of the cat visual cortex. Brain Res 289:143–155

    Article  CAS  PubMed  Google Scholar 

  • Singer W (1977) Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiol Rev 57:386–420

    CAS  PubMed  Google Scholar 

  • Singer W (1979) Central-core control of visual cortex functions. In: Schmitt FO, Worden FG (eds) The neurosciences fourth study program, MIT, Cambridge, Mass., pp 1093–1110

    Google Scholar 

  • Steriade M, Biesold D (eds) (1990) Brain cholinergic systems, Oxford University Press, Oxford

    Google Scholar 

  • Stewart DJ, MacFabe DF, Vanderwolf CH (1984) Cholinergic activation of the electrocorticogram: role of the substantia innominata and effects of atropine and quinuclidinyl benzilate. Brain Res 322:219–232

    Article  CAS  PubMed  Google Scholar 

  • Stichel CC, Singer W (1985) Organization and morphological characteristics of choline acetyltransferase-containing fibers in the visual thalamus and striate cortex of the cat. Neurosci Lett 53:155–160

    Article  CAS  PubMed  Google Scholar 

  • Stichel CC, Singer W (1987) Quantitative analysis of the choline acetyltransferase-immunoreactive axonal network in the cat primary visual cortex. I. Adult cats. J Comp Neurol 258:91–98

    Article  CAS  PubMed  Google Scholar 

  • Swanson LW (1976) An autoradiographic study of the efferent conections of the preoptic region in the rat. J Comp Neurol 167:227–256

    Article  CAS  PubMed  Google Scholar 

  • Tomimoto H, Kamo H, Kameyama M, McGeer P, Kimura H (1987) Descending projections of the basal forebrain in the rat demonstrated by the anterograde neural tracer Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 425:248–255

    Article  CAS  PubMed  Google Scholar 

  • Vanderwolf CH (1987) Near-total loss of ‘learning’ and ‘memory’ as a result of combined cholinergic and serotonergic blockade in the rat. Behav Brain Res 23:43–57

    Article  CAS  PubMed  Google Scholar 

  • Vertes RP (1988) Brainstem afferents to the basal forebrain in the rat. Neuroscience 24:907–935

    Article  CAS  PubMed  Google Scholar 

  • Vincent SR, Reiner PB (1987) The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371–415

    Article  CAS  PubMed  Google Scholar 

  • Wahle P, Sanides-Buchholtz C, Eckenstein F, Albus K (1984) Concurrent visualization of choline acetyltransferase like immunoreactivity and retrograde transport of neocortically injected markers in basal forebrain neurons of cat and rat. Neurosci Lett 44:223–228

    Article  CAS  PubMed  Google Scholar 

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Müller, C.M., Lewandowski, M.H. & Singer, W. Structures mediating cholinergic reticular facilitation of cortical responses in the cat: effects of lesions in immunocytochemically characterized projections. Exp Brain Res 96, 8–18 (1993). https://doi.org/10.1007/BF00230434

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  • DOI: https://doi.org/10.1007/BF00230434

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