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Role of the Basal Forebrain Cholinergic System in Cortical Activation and Arousal

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Activation to Acquisition

Abstract

A basic question about the physiology of the cerebral cortex concerns the activating afferents that keep the neocortex in the aroused or waking state. Imbedded in this question are several other questions: Why must the cerebral cortex be aroused in the first place in order to interact with the environment? Why is the brain not hard-wired exclusively for the information processing mode, as seen in computers? What is the biological significance of the dichotomy of the activated (open-loop) and non-activated (closed-loop) states of the cerebral hemispheres? And finally, what are the neurophysiological mechanisms involved in the switching between the diametrically opposite functional states? This last question, as we will discuss it in this chapter, is under intensive investigation and clarification, whereas little work or even speculation is appearing on the evolutionary advantage of the functional dichotomy of the brain (Buzsáki, 1989).

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References

  • Arendash, G., Millard, W.J., Dunn, A.J. and Meyer, E.M. (1987): Long-term neuropathological and neurochemical effects of nucleus basalis lesions in the rat. Science 238:952–956

    Article  Google Scholar 

  • Asanuma, C. (1989): Magnocellular basal nucleus projection to the thalamic reticular nucleus in rats: a structural substrate for the thalamic modulation of thalamic excitability by the basal forebrain. Proc. Natl. Acad. Sci. 86:4746–4750

    Article  Google Scholar 

  • Aston-Jones, G. and Bloom, F.E. (1981): Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious stimuli. J. NeuroSci. 1:887–900

    Google Scholar 

  • Aston-Jones, G., Shaver, R. and Dinan, T.G. (1984): Cortically projecting nucleus basalis neurons in rat are physiologically heterogeneous. Neurosci. Lett. 46:19–24

    Article  Google Scholar 

  • Ball, G.J., Gloor, P. and Schaul, N. (1977): The cortical electromicrophysiology of cats. Electroencephal. Clin. Neurophysiol. 43:46–363

    Google Scholar 

  • Belardetti, E., Borgia, R., and Mancia, M. (1977): Prosencephalic mechanisms of ECoG desynchronization in cerveau isole cats. Electroencephal. Clin. Neurophysiol. 42:213–225

    Article  Google Scholar 

  • Benardo, L.S. and Prince, D.A. (1982): Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249:315–331

    Article  Google Scholar 

  • Buzsáki, G. (1989): Two-stage model of memory trace formation: a role for “noisy” brain states. NeuroSci. 31:551–570

    Article  Google Scholar 

  • Buzsáki, G., Bickford, T.G., Ponomareff, G., Thal, L.J., Mandel, R.J. and Gage, F.H. (1988a): Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. NeuroSci. 8:4007–4026

    Google Scholar 

  • Buzsáki, G., Bickford, R.G., Armstrong, D.M., Ponomareff, G., Chen, K., Ruiz, R., Thal, L.J. and Gage, R.H. (1988b): EEG activity in the neocortex of freely moving young and aged rats. NeuroSci. 26:735–744

    Article  Google Scholar 

  • Buzsáki, G., Ponomareff, G., Bayardo, F., Shaw, T. and Gage, F.H. (1988c): Suppression and induction of epileptic activity by neuronal grafts. Proc. Natl. Acad. Sci. 85:9327–9330

    Article  Google Scholar 

  • Buzsáki, G., Smith, A., Berger, S. Fisher, L.J. and Gage, F.H. (1990): Petit mal epilepsy and parkinsonian tremor: hypothesis of a common pacemaker. NeuroSci. in press

    Google Scholar 

  • Calvet, J. and Fourment, Michel T. (1973): Electrical activity in neocortical projection and association areas during slow wave sleep. Brain Res. 5:173–187

    Article  Google Scholar 

  • Casamenti, F., Defenu, G., Abbamondi, A. L. and Pepeu, G. (1986): Changes in cortical acetylcholine output induced by modulation of the nucleus basalis. Brain Res. Bull. 16:689–695

    Article  Google Scholar 

  • Coben, L.A., Danzinger, W.L. and Starandt, M. (1985): A longitudinal study of mild senile dementia of Alzheimer type: changes at 1 year and 2.5 years. Electroencephal Clin. Neurophysiol. 61:101–112

    Article  Google Scholar 

  • Cole, A.E. and Nicoll, R.A. (1984): Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. J. Physiol. (Lond) 352:173–188

    Google Scholar 

  • Creutzfeldt, O., Watanabe, S. and Lux, H.D. (1966): Relations between EEG phenomena and potentials of single cortical cells. I. Evoked responses after thalamic and epicortical stimulation. Electroencephal. Clin. Neurophysiol. 20:1–18

    Article  Google Scholar 

  • DeLong, M. R. (1971): Activity of pallidal neurons during movement. J. Neurophysiol. 34:414–427

    Google Scholar 

  • Detarí, L., Juhasz, G. and Kukorelli, T. (1984): Firing properties of cat basal fore-brain neurons during sleep-wakefulness cycles. Electroenceph. Clin. Neurophysiol. 58:362–368

    Article  Google Scholar 

  • Detari, L. and Vanderwolf, C.H. (1987): Activity of identified cortically projecting and other basal forebrain neurons during large slow waves and cortical activation in anesthetized rats. Brain Res. 437:1–10

    Article  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  Google Scholar 

  • Fibiger, H.C. (1982): The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res. Rev. 4:327–388

    Article  Google Scholar 

  • Foote, S.L., Aston-Jones, G. and Bloom, F.E. (1980): Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc. Natl. Acad. Sci. 77:3033–3037

    Article  Google Scholar 

  • Fox, K. and Armstrong-James, M. (1986): The role of the anterior intralaminar nuclei and N-methyl D-aspartate receptors in the generation of spontaneous bursts in rat neocortical neurones. Exp. Brain Res. 63:505–518

    Article  Google Scholar 

  • Funahashi, S. (1983): Responses of monkey prefrontal neurons during a visual tracking task reinforced by substantia innominata self-stimulation. Brain Res. 276:267–276

    Article  Google Scholar 

  • Griffith, W.H. and Matthews, R.T. (1986): Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci. Lett. 71:171–174

    Article  Google Scholar 

  • Haas, H.L. and Konnerth, A. (1983): Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature (Lond.) 302:432–434

    Article  Google Scholar 

  • Hallanger, A. E., Levey, A. I., Lee, H. J., Rye, D. B. and Wainer, B. H. (1987): The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. Comp. Neurol. 262:105–124

    Article  Google Scholar 

  • Jahnsen, H. and Llinas, R. (1984): Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. (Lond.) 349: 205–226

    Google Scholar 

  • Jasper, H.H. (1949): Diffuse projection systems: the integrative action of the thalamic reticular system. Electroenceph. Clin. Neurophysiol. 1:405–420

    Google Scholar 

  • Jones, E.G. (1985): The Thalamus. New York: Plenum Publishing Corp.

    Google Scholar 

  • Jones, E.G., Burton, H., Saper, C.B. and Swanson, L.W. (1976): Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J. Comp. Neurol. 167:385–420

    Article  Google Scholar 

  • Klingberg, F. and Pickenhain, L. (1968): Das Aufreten von ‘Spindelenthadinigen’ bei der ratte in Beziehung zum Verhalten. Acta Biol. Med. Germ. 20:45–54

    Google Scholar 

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

    Google Scholar 

  • Lamour, Y., Dutar, P., Rascol, O. and Joberts, A. (1986): Basal forebrain neurons projecting to the rat fronto-parietal cortex: electrophysiological and pharmacological properties. Brain Res. 362:122–131

    Article  Google Scholar 

  • Llinas, R.R. (1988): The intrinsic electrophysiological properties of mammalian neurons: insight into central nervous system. Science 242:1654–1664

    Article  Google Scholar 

  • Lo Conte, G., Casamenti, E., Bigl, V., Milaneschi, E. and Pepeu, G. (1982): Effect of magnocellular forebrain nuclei lesions on acetylcholine output from the cerebral cortex, electrocorticogram and behavior. Arch. Ital. Biol. 120:176–188

    Google Scholar 

  • Longo, V.G. (1956): Effects of scopolamine and atropine on electro-encephalo-graphic and behavioral reactions due to hypothalamic stimulation. J. Pharmacol. 116:198–208

    Google Scholar 

  • Madison, D.V. and Nicoll, R.A. (1986): Actions of noradrenaline recorded in-tracellularly in rat hippocampal CA1 pyramidal neurons, in vitro. J. Physiol. (Lond.) 321:175–177

    Google Scholar 

  • McCormick, D.A. and Prince, D.A. (1986): Mechanisms of action of acetylcholine in the guinea pig cerebral cortex in vitro. J. Neurophysiol. 375:169–194

    Google Scholar 

  • McGinty, D.J. and Sterman, M.B. (1968): Sleep suppression after basal forebrain lesions in cat. Science 160:1253–1255

    Article  Google Scholar 

  • Mesulam, M.-M. and Van Hoesen, G.W. (1976): Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex. Brain Res. 109:152–157

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E.J., Wainer, B.H. and Levey, A.I. (1983): Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Chl-Ch6). NeuroSci. 4:1185–1201

    Article  Google Scholar 

  • Mitchell, S.J., Richardson, R.T. and DeLong, M.R. (1987a): The primate globus pallidus: neuronal activity related to direction of movement. Exp. Brain. Res. 68:491–505

    Google Scholar 

  • Mitchell, S.J., Richardson, R.T. and DeLong, M.R. (1987b): The primate nucleus basalis: neuronal activity related to behavior. Exp. Brain Res. 68:506–515

    Google Scholar 

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

    Google Scholar 

  • Nakajima, Y., Nakajima, S., Leonard, R.J. and Yamaluchi, K. (1986): Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc. Natl. Acad. Sci. 83:3022–3026

    Article  Google Scholar 

  • Nicoll, R.A. (1988): The coupling of neurotransmitter receptors to ion channels in the brain. Science 241:545–551

    Article  Google Scholar 

  • Papez, J.W. (1956): Central reticular path to intralaminar and reticular neurons of the thalamus for activating EEG related to consciousness. Electroencephal. Clin. Neurophysiol. 8:117–128

    Article  Google Scholar 

  • Pentilla, M., Partanen, J.V., Soinen, H. and Riekkinen, P. J. (1985): Quantitative analysis of occipital EEG in different stages of Alzheimer’s disease. Electroencephal. Clin. Neurophysiol. 60:1–6

    Article  Google Scholar 

  • Phillis, J.W. (1980): Acetylcholine release from the cerebral cortex and its role in cortical arousal. Brain Res. 7:378–389

    Article  Google Scholar 

  • Rappelsberger, P., Pockberger, H. and Petsche, H. (1981): The contribution of the cortical layers to the generation of the EEG: field potential and current source density analyses in the rabbit’s visual cortex. Electroenceph. Clin. Neurophysiol. 53:254–269

    Article  Google Scholar 

  • Reiner, P.B., Semba, K., Fibiger, H.C. and McGeer, E.G. (1987): Physiological evidence for subpopulations of cortically projecting basal forebrain neurons in the anesthetized rat. NeuroSci. 20:629–636

    Article  Google Scholar 

  • Ribak, C.E. (1978): Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats containing glutamic acid decarboxylase. J. Neurocytol. 7:461–478

    Article  Google Scholar 

  • Richardson, R.T. and DeLong, M.R. (1988): A reappraisal of the functions of the nucleus basalis of Meynert. Trends NeuroSci. 11:264–267

    Article  Google Scholar 

  • Richardson, R.T., Mitchell, S.J., Baker, F.H. and DeLong, M.R. Responses of

    Google Scholar 

  • nucleus basalis of Meynert neurons in behaving monekys. In: Cellular Mechanisms of Conditioning and Behavioral Plasticity. C.D. Woody, D.L. Alkon and McGaugh, J.L., eds. New York: Plenus Publishing Corp. pp 161–173

    Google Scholar 

  • Rigdon, G.C. and Pirch, J.H. (1986): Nucleus basalis involvement in conditioned neuronal responses in the rat frontal cortex. J. NeuroSci. 6:2535–2542

    Google Scholar 

  • Rolls, E.T., Sanghera, M.K. and Roper-Hall, A. (1979): The latency of activation of neurons in the lateral hypothalamus and substantia innominata during feeding in the monkey. Brain Res.l64:121–135

    Article  Google Scholar 

  • Semba, K., Reiner, P.B., McGeer, E.G. and Fibiger, H.C. (1987): Morphology of cortically projecting basal forebrain neurons in the rat as revealed by intracellular iontophoresis of horseradish Peroxydase. NeuroSci. 20:637–351

    Article  Google Scholar 

  • Shute, C. D. and Lewis, P. R. (1967): The ascending cholinergic reticular systems: neocortical, olfactory and subcortical projections. Brain 90:497–520

    Article  Google Scholar 

  • Siegel, J., and Wang, R.Y. (1974): Electroencephalographic, behavioral and single-unit effects produced by stimulation of forebrain inhibitory structures in cats. Exp. Neurol. 42:28–50

    Article  Google Scholar 

  • Somogyi, P., Kisvarday, Z.F., Martin, K.A.C. and Whitteridge, D. (1983): Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. NeuroSci. 10:261–294

    Article  Google Scholar 

  • Steriade, M. (1970): Ascending control of thalamic and cortical responsiveness. Int. Rev. Neurobiol. 12:87–144

    Article  Google Scholar 

  • Steriade, M. and Buzsáki, G. (1989): Parallel activation of thalamic and cortical neurons by brainstem and forebrain cholinergic systems. In: Brain Cholinergic Systems. Steriade, M., Biesold, D., eds. Oxford: Oxford University Press

    Google Scholar 

  • Steriade, M. and Deschenes, M. (1988): The thalamus as a neuronal oscillator. Brain Res. Rev. 8:1–63

    Article  Google Scholar 

  • Steriade, M. and Llinas, R. (1988): The functional states of the thalamus and the associated neuronal interplay. Physiol. Rev. 68:649–742

    Google Scholar 

  • Steriade, M., Parent, A., Paré, D. and Smith, Y. (1987): Cholinergic and non-cholinergic neurons of the cat basal forebrain project to reticular and mediodorsal thalamic nuclei. Brain Res. 408:372–376

    Article  Google Scholar 

  • Sterman, M.B. and Clemente, C.D. (1962): Forebrain inhibitory mechanisms: sleep patterns induced by forebrain stimulation in the behaving cat. Exp. Neurol. 6:103–117

    Article  Google Scholar 

  • Stern, W.C. and Pugh, W.W. (1984): Responses of frontal cortex single units to magnocellular basal forebrain stimulation. Soc. Neurosci. Abstr. 10:9.

    Google Scholar 

  • Stewart, D.J., MacFabe, D.F. and Vanderwolf, C.H. (1984): Cholinergic activation of the electrocorticogram: role of substantia innominata and effects of atropine and quinuclidinyl benzylate. Brain Res. 322:219–232

    Article  Google Scholar 

  • Szymusiak, D. and McGinty, D. (1986): Sleep-related neuronal discharge in the basal forebrain of cats. Brain Res. 370:82–92

    Article  Google Scholar 

  • Traub, R.D., Miles, R. and Wong, R.K.S. (1989): Model of rhythmic population oscillation in the hippocampal slice. Science 243:1319–1325

    Article  Google Scholar 

  • Trulson, M.E. and Jacobs, B.L. (1979): Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res. 163:135–150

    Article  Google Scholar 

  • Vanderwolf, C.H. (1975): Neocortical and hippocampal activation in relation to behavior: effects of atropine, eserine, phenothiazines, and amphetamine. J. Comp. Physiol Psychol 88:300–323

    Article  Google Scholar 

  • Vanderwolf, C.H. (1988): Cerebral activity and behavior: control by central cholinergic and serotonergic systems. Intl. Rev. Neurobiol 30:225–340

    Article  Google Scholar 

  • Vanderwolf, C.H. and Baker, G.B. (1986): Evidence that serotonin mediates non-cholinergic neocortical low voltage fast activity, non-cholinergic hippocampal rhythmical slow activity and contributes to intelligent behavior. Brain Res. 374:342–356

    Article  Google Scholar 

  • Vanderwolf, C.H. and Robinson, T.H. (1981): Reticulocortical activity and behavior: a critique of the arousal theory and a new synthesis. Behav. Brain Sci. 4:459–514

    Article  Google Scholar 

  • Vanderwolf, C.H. and Stewart, D.J. (1986): Joint cholinergic-serotonergic control of neocortical and hippocampal electrical activity in relation to behavior: effects of scopolamine, ditran, trifluoperazine and amphetamine. Physiol Behav. 38:57–65

    Article  Google Scholar 

  • Vanderwolf, C.H. and Steward, D.J. (1988): Thalamic control of neocortical activation: a critical re-evaluation. Brain Res. Bull 20:529–53

    Article  Google Scholar 

  • Wikler, A. (1952): Pharmacologic dissociation on behavior and EEG sleep patterns in dogs: morphine, N-allylnormorphine and atropine. Proc. Soc. Exp. Biol., N.Y. 79:261–266

    Google Scholar 

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Buzsáki, G., Gage, F.H. (1991). Role of the Basal Forebrain Cholinergic System in Cortical Activation and Arousal. In: Richardson, R.T. (eds) Activation to Acquisition. Birkhäuser, Boston, MA. https://doi.org/10.1007/978-1-4684-0556-9_5

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  • DOI: https://doi.org/10.1007/978-1-4684-0556-9_5

  • Publisher Name: Birkhäuser, Boston, MA

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