Increases in hippocampal and frontal cortical acetylcholine release associated with presentation of sensory stimuli

In vivo microdialysis was employed to monitor acetylcholine release in the hippocampus and frontal cortex of freely behaving rats. Four stimuli were presented on separate occasions in the course of a dialysis session to rats with microdialysis probes implanted in the hippocampus or frontal cortex. Visual, auditory, olfactory and tactile stimuli elicited a number of different responses such as exploratory and consummatory behaviours. Presentation of two of the stimuli (auditory and tactile) also produced periods of alert immobility (freezing). All of the stimuli increased acetylcholine release in both the hippocampus and cortex: in the hippocampus, this increase was statistically significant with all except the olfactory stimulus, whereas in the cortex all but the visual stimulus resulted in significant increases. In the hippocampus, there were no significant differences between the increases in acetylcholine release produced by the four stimuli. In contrast, in the cortex, there was significant variation between the magnitude of acetylcholine release produced by the different stimuli: acetylcholine release elicited by tactile stimulation was greater than that produced by the other stimuli. There was no significant variation in the duration of increases in acetylcholine release produced by the stimuli in either the hippocampus or cortex. These results provide evidence that acetylcholine release is associated with a variety of behavioural responses to stimuli designed to produce arousal, and point to a role for cortical and hippocampal cholinergic mechanisms in arousal or attention. Further, the results suggest that under some circumstances cortical and hippocampal acetylcholine release may be regulated differentially.

[1]  Gastone G. Celesia,et al.  Acetylcholine released from cerebral cortex in relation to state of activation , 1966, Neurology.

[2]  I. Whishaw,et al.  Release of acetylcholine from the hippocampus of freely moving rats during sensory stimulation and running , 1979, Neuropharmacology.

[3]  C. L. Cox,et al.  Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[5]  M. Frotscher,et al.  Central Cholinergic Synaptic Transmission , 1989, Experientia Supplementum.

[6]  Barry R. Komisaruk,et al.  Synchrony among rhythmical facial tremor, neocortical ‘ALPHA’ waves, and thalamic non-sensory neuronal bursts in intact awake rats , 1980, Brain Research.

[7]  H. Fibiger,et al.  Dopaminergic Regulation of Septohippocampal Cholinergic Neurons , 1994, Journal of neurochemistry.

[8]  D. McCormick,et al.  Mechanisms of action of acetylcholine in the guinea‐pig cerebral cortex in vitro. , 1986, The Journal of physiology.

[9]  A. Björklund,et al.  Acetylcholine release in the rat hippocampus as studied by microdialysis is dependent on axonal impulse flow and increases during behavioural activation , 1990, Neuroscience.

[10]  Vanderwolf Ch,et al.  Neocortical and hippocampal activation in relation to behavior: Effects of atropine, eserine, phenothiazines, and amphetamine. , 1975 .

[11]  P. Mcgeer,et al.  Aging, Alzheimer's disease, and the cholinergic system of the basal forebrain , 1984, Neurology.

[12]  R. Dykes,et al.  Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. , 1990, Journal of neurophysiology.

[13]  H. Fibiger,et al.  Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: An in vivo microdialysis study , 1991, Pharmacology Biochemistry and Behavior.

[14]  J S Schwaber,et al.  Distribution and organization of cholinergic neurons in the rat forebrain demonstrated by computer‐aided data acquisition and three‐dimensional reconstruction , 1987, The Journal of comparative neurology.

[15]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  J. Coyle,et al.  Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. , 1982, Science.

[17]  O D Creutzfeldt,et al.  Crosscorrelation between the activity of septal units and hippocampal EEG during arousal. , 1974, Brain research.

[18]  ML Voytko,et al.  Basal forebrain lesions in monkeys disrupt attention but not learning and memory [published erratum appears in J Neurosci 1995 Mar;15(3): following table of contents] , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  R. Nicoll,et al.  Characterization of a slow cholinergic post‐synaptic potential recorded in vitro from rat hippocampal pyramidal cells. , 1984, The Journal of physiology.

[20]  O. Steward,et al.  Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  G. Buzsáki,et al.  The cholinergic nucleus basalis: a key structure in neocortical arousal. , 1989, EXS.

[22]  H. Teitelbaum,et al.  Behaviorally evoked hippocampal theta waves: a cholinergic response. , 1975, Science.

[23]  M. Kurosawa,et al.  Extracellular release of acetylcholine, noradrenaline and serotonin increases in the cerebral cortex during walking in conscious rats , 1993, Neuroscience Letters.

[24]  J. D. Dudar.  The role of the septal nuclei in the release of acetylcholine from the rabbit cerebral cortex and dorsal hippocampus and the effect of atropine , 1977, Brain Research.

[25]  J. Szerb.  Cortical acetylcholine release and electroencephalographic arousal , 1967, The Journal of physiology.

[26]  T. Robinson,et al.  Effects of hemicholinium-3 and choline on hippocampal electrical activity during immobility vs. movement. , 1980, Electroencephalography and clinical neurophysiology.

[27]  B. Everitt,et al.  AMPA-induced excitotoxic lesions of the basal forebrain: a significant role for the cortical cholinergic system in attentional function , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  T. Robbins,et al.  Comparative effects of ibotenic acid- and quisqualic acid-induced lesions of the substantia innominata on attentional function in the rat: further implications for the role of the cholinergic neurons of the nucleus basalis in cognitive processes , 1989, Behavioural Brain Research.

[29]  R. Dykes,et al.  Daily changes in the release of acetylcholine from rat primary somatosensory cortex , 1993, Brain Research.

[30]  T. Robinson,et al.  Microdialysis in the neurosciences , 1991 .

[31]  H. Fibiger,et al.  Enhanced acetylcholine release in hippocampus and cortex during the anticipation and consumption of a palatable meal , 1994, Neuroscience.

[32]  R. Dykes,et al.  Long-term enhancement of evoked potentials in raccoon somatosensory cortex following co-activation of the nucleus basalis of Meynert complex and cutaneous receptors , 1991, Brain Research.

[33]  B. Sahakian,et al.  The Effects of Nicotine on Attention, Information Processing, and Short-Term Memory in Patients with Dementia of the Alzheimer Type , 1989, British Journal of Psychiatry.

[34]  Y. Endo,et al.  Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation , 1991, Neuroscience.

[35]  G. Damsma,et al.  Measurement of Acetylcholine Release in Freely Moving Rats by Means of Automated Intracerebral Dialysis , 1987, Journal of neurochemistry.

[36]  R. Miettinen,et al.  Effects of quisqualic acid nucleus basalis lesioning on cortical EEG, passive avoidance and water maze performance , 1990, Brain Research Bulletin.

[37]  J. Pirch,et al.  A role for acetylcholine in conditioning-related responses of rat frontal cortex neurons: microiontophoretic evidence , 1992, Brain Research.

[38]  C. H. Vanderwolf,et al.  Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: Relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital , 1975, Experimental Neurology.

[39]  H. Soininen,et al.  Quantitative analysis of occipital EEG in different stages of Alzheimer's disease. , 1985, Electroencephalography and clinical neurophysiology.

[40]  J. Edeline,et al.  Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat , 1993, Neuroscience.

[41]  TATSUYA KANAI,et al.  Mesencephalic Reticular Activating System and Cortical Acetylcholine Output , 1965, Nature.

[42]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[43]  D. German,et al.  Neuronal pathology in the nucleus basalis and associated cell groups in senile dementia of the Alzheimer's type , 1985, Neurology.

[44]  C. H. Vanderwolf.  Cerebral activity and behavior: control by central cholinergic and serotonergic systems. , 1988, International review of neurobiology.

[45]  John P. Donoghue,et al.  Cholinergic modulation of sensory responses in rat primary somatic sensory cortex , 1987, Brain Research.