Abstract
Neurons in the locus coeruleus (LC) encode information related to behavioral state in a tonic pattern of firing and information related to the occurrence of a sensory stimulus in a phasic pattern of firing. The effects of phasic stimulation of the LC (6 pulses at 30 Hz), designed to approximate its physiological activation by sensory stimuli, were studied in the lateral geniculate nucleus (LGN) of anesthetized rats. Phasic stimulation of the LC significantly increased neuronal firing in the LGN with a mean latency 320 ms from onset of stimulation. Receiver operating characteristic analyses on a trial-by-trial basis showed that phasic LC stimulation can result in a highly discriminable signal in the LGN. This increased neuronal firing rate in the LGN was specific for the site of stimulation and was reduced by the norepinephrine synthesis inhibitor α-methyl-p-tyrosine and by intravenous WB-4101 (α1-receptor antagonist). Neurons in the LGN have a single-spike firing mode when sensory information is faithfully relayed from retina to cortex and a burst-firing mode when the transfer of this information is degraded. Phasic LC stimulation reduced burst firing (2–5 ms interspike intervals, ISIs) at low frequencies (≤4 Hz) in the LGN, and for some neurons there was an absolute decrease in burst-like ISIs after LC stimulation, despite an increase in mean firing rate.
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References
Aston-Jones G (1985) Behavioral functions of locus coeruleus derived from cellular attributes. Physiol Psychol 13:118–126
Aston-Jones G, Bloom FE (1981a) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuation in the sleep-waking cycle. J Neurosci 1:876–886
Aston-Jones G, Bloom FE (1981b) Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1:887–900
Chan OL, Webster RA (1971) Importance of noradrenaline found in a functional pool in maintaining spontaneous locomotor activity in rats. Br J Pharmacol 41:700–708
Cohn TE, Green DG, Tanner WP (1975) Receiver operating characteristic analysis. Application to the study of quantum fluctuation effects in optic nerve of Rana pipiens. J Gen Physiol 66:583–616
Crunelli V, Kelly JS, Leresche N, Pirchio M (1987) The ventral and dorsal lateral geniculate nucleus of the rat: intracellular recordings in vitro. J Physiol (Lond) 384:587–601
Funke K, Pape HC, Eysel UT (1993) Noradrenergic modulation of retinogeniculate transmission in the cat. J Physiol (Lond) 463:169–191
Gibson S, McGeer EG, McGeer PL (1970) Effect of selective inhibitors of tyrosine and tryptophan hydroxylases on self-stimulation in the rat. Exp Neurol 27:283–290
Goldstein M, Nakajima K (1967) The effect of disulfiram on catecholamine levels in the brain. J Pharm Exp Ther 157:96–102
Harley C, Milway JS, Lacaille JC (1989) Locus coeruleus potentiation of dentate gyrus responses: evidence for two systems. Brain Res Bull 22:643–650
Holdefer RN, Jensen RA (1987) The effects of peripheral d-amphetamine, 4-OH amphetamine, and epinephrine on maintained discharge in the locus coeruleus with reference to the modulation of learning and memory by these substances. Brain Res 417:108–117
Holdefer RN, Norton TT, Godwin DG (1989) Effects of bicuculline on signal detectability in lateral geniculate nucleus relay cells. Brain Res 488:341–347
Jacobs BL (1990) Locus coeruleus neuronal activity in behaving animals. In: Heal DJ, Marsden CJ (eds) The pharmacology of noradrenaline in the central nervous system. Oxford University Press, Oxford, pp 248–265
Jahnsen H, Llinas R (1984a) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol (Lond) 349:205–226
Jahnsen H, Llinas R (1984b) Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol (Lond) 349:227–247
Kayama Y (1985) Ascending, descending and local control of neuronal activity in the rat lateral geniculate nucleus. Vision Res 25:339–347
Kayama Y, Negi T, Sugitani M, Iwama K (1982) Effects of locus coeruleus stimulation on neuronal activities of dorsal lateral geniculate nucleus and perigeniculate reticular nucleus of the rat. Neuroscience 7:655–666
Kayama Y, Takagi M, Ogawa T (1986) Cholinergic influence of the laterodorsal tegmental nucleus on neuronal activity in the rat lateral geniculate nucleus. J Neurophysiol 56:1297–1309
Kromer LF, Moore RY (1980) A study of the organization of the locus coeruleus projections to the lateral geniculate nuclei of the albino rat. Neuroscience 5:255–271
Leresche N, Lightowler S, Soltesz I, Jassik-Gerschenfeld D, Crunelli V (1991) Low-frequency oscillatory activities intrinsic to rat and cat thalamocortical cells. J Physiol (Lond) 441:155–174
Lindvall O, Bjorklund A, Nobin A, Stenevi U (1974) The adrenergic innervation of the rat thalamus as revealed by the glyoxylic acid fluorescence method. J Comp Neurol 154:317–348
Livingstone MS, Hubel DH (1981) Effects of sleep and arousal on the processing of visual information in the cat. Nature 291:554–561
Lundberg JM, Rudehill A, Sollevi A, Theodorsson-Norheim E, Hamberger B (1986) Frequency-dependent and reserpine-dependent chemical coding of sympathetic neurotransmission-differential release of noradrenaline and neuropeptide Y from pig spleen. Neurosci Lett 63:96–100
McCormick DA, Feeser HR (1990) Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39:103–113
McCormick DA, Pape H-C (1990a) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol (Lond) 431:291–318
McCormick DA, Pape H-C (1990b) Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. J Physiol (Lond) 431:319–342
Nakai Y, Takaori S (1974) Influence of norepinephrine-containing neurons derived from the locus coeruleus on lateral geniculate neuronal activities of cats. Brain Res 71:47–60
Nicholls JG, Martin AR, Wallace BG (1992) From neuron to brain. Sinauer, Sunderland, Mass.
Papadopoulos GC, Parnavelas JG (1990) Distribution and synaptic organization of serotoninergic and noradrenergic axons in the lateral geniculate nucleus of the rat. J Comp Neurol 294:345–355
Rainbow TC, Parsons B, Wolfe BB (1984) Quantitative autoradiography of β1- and β2-adrenergic receptors in rat brain. Proc Natl Acad Sci USA 81:1585–1589
Rogawski MA, Aghajanian GK (1982) Activation of lateral geniculate neurons by locus coeruleus or dorsal noradrenergic bundle stimulation: selective blockade by the alpha11-adrenoceptor antagonist prazosin. Brain Res 205:31–39
Rasmussen K, Morilak DA, Jacobs BL (1986a) Single unit activity of locus coeruleus neurons in the freely moving cat. I. During naturalistic behaviors and in response to simple and complex stimuli. Brain Res 371:324–334
Rasmussen K, Strecker RE, Jacobs BL (1986b) Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli. Brain Res 369:336–340
Sargent Jones L, Gauger LL, Davis JN (1985) Anatomy of brain alpha1-adrenergic receptors: in vitro autoradiography with [125I]-Heat. J Comp Neurol 231:190–208
Sato H, Fox K, Daw NW (1989) Effect of electrical stimulation of locus coeruleus on the activity of neurons in the cat visual cortex. J Neurophysiol 62:946–958
Seabrook GR, Duce IR, Irving SN (1989) Spontaneous and evoked quantal neurotransmitter release at the neuromuscular junction of the larval housefly, Musca domestica. Pflugers Arch 414:44–51
Soltesz I, Lightowler S, Leresche N, Jassik-Gerschenfeld D, Pollard CE, Crunelli V (1991) Two inward currents and the transformation of low-frequency oscillations of rat and cat thalamocortical cells. J Physiol (Lond) 441:175–197
Steriade M, Llinas R (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742
Steriade M, Curro Dossi R, Nunez A (1991) Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortical potentiation and brainstem cholinergic suppression. J Neurosci 11:3200–3218
Swets JA, Tanner WP, Birdsall TG (1964) Decision processes in perception. In: Swets JA (ed) Signal detection and recognition by human observers. Wiley, New York
Woodward DJ, Moises HC, Waterhouse BD, Yeh HH, Cheun JE (1991) Modulatory actions of norepinephrine on neural circuits. In: Kito et al. (ed) Neuroreceptor mechanisms in brain. Plenum, New York
Woolf NJ, Butcher LL (1986) Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603–637
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Holdefer, R.N., Jacobs, B.L. Phasic stimulation of the locus coeruleus: effects on activity in the lateral geniculate nucleus. Exp Brain Res 79, 444–452 (1994). https://doi.org/10.1007/BF00229184
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DOI: https://doi.org/10.1007/BF00229184