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Differential Afferent Regulation of the Basal Forebrain by Telencephalic and Brainstem Afferents

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Differential Afferent Regulation of the Basal Forebrain by Telencephalic and Brainstem Afferents Cortical ACh in attention and dreaming Neuroscience Vol. 95, No. 4, pp. 933–952, 2000933 Copyright q 1999 IBRO. Published by Elsevier Science Ltd Pergamon Printed in Great Britain. All rights reserved PII: S0306-4522(99)00487-X 0306-4522/00 $20.00+0.00 www.elsevier.com/locate/neuroscience COMMENTARY CORTICAL CHOLINERGIC INPUTS MEDIATING AROUSAL, ATTENTIONAL PROCESSING AND DREAMING: DIFFERENTIAL AFFERENT REGULATION OF THE BASAL FOREBRAIN BY TELENCEPHALIC AND BRAINSTEM AFFERENTS M. SARTER* and J. P. BRUNO Department of Psychology, The Ohio State University, 27 Townshend Hall, Columbus, OH 43210, U.S.A. Abstract—Basal forebrain corticopetal neurons participate in the mediation of arousal, specific attentional functions and rapid eye movement sleep-associated dreaming. Recent studies on the afferent regulation of basal forebrain neurons by telencephalic and brainstem inputs have provided the basis for hypotheses which, collectively, propose that the involvement of basal forebrain corticopetal projections in arousal, attention and dreaming can be dissociated on the basis of their regulation via major afferent projections. While the processing underlying sustained, selective and divided attention performance depends on the integrity of the telencephalic afferent regulation of basal forebrain corticopetal neurons, arousal-induced attentional processing (i.e. stimulus detection, selection and processing as a result of a novel, highly salient, aversive or incentive stimuli) is mediated via the ability of brainstem ascending noradrenergic projections to the basal forebrain to activate or “recruit” these telencephalic afferent circuits of the basal forebrain. In rapid eye movement sleep, both the basal forebrain and thalamic cortiocopetal projections are stimulated by cholinergic afferents originating mainly from the pedunculopontine and laterodorsal tegmenta in the brainstem. Rapid eye movement sleep-associated dreaming is described as a form of hyperattentional processing, mediated by increased activity of cortical cholinergic inputs and their cortical interactions with activated thalamic efferents. In this context, long-standing specula- tions about the similarities between dreaming and psychotic cognition are substantiated by describing the role of an over(re)active cortical cholinergic input system in either condition. Finally, while determination of the afferent regulation of basal forebrain corticopetal neurons in different behavioral/cognitive states assists in defining the general cognitive functions of cortical acetylcholine, this research requires a specification of the precise anatomical organization of basal forebrain afferents and their interactions in the basal forebrain. Furthermore, the present hypoth- eses remain incomplete because of the paucity of data concerning the regulation and role of basal forebrain non-cholinergic, particularly GABAergic, efferents. q 1999 IBRO. Published by Elsevier Science Ltd. Key words: basal forebrain, acetylcholine, brainstem, thalamus, attention, dreaming. CONTENTS 1. INTRODUCTION 934 2. BEHAVIORAL AROUSAL AND ATTENTIONAL PERFORMANCE: CONCEPTUAL OVERLAPS AND DIFFERENCES 934 3. DISSOCIATIONS AND INTERACTIONS BETWEEN TELENCEPHALIC AND BRAINSTEM PROJECTIONS TO BASAL FOREBRAIN NEURONS IN AROUSAL AND ATTENTION 935 3.1. GABAergic afferents originating from the nucleus accumbens: from motivation to attention to action 935 3.2. Glutamatergic afferents: telencephalic stimulation of basal forebrain corticopetal projections in attention 937 3.3. Telencephalic afferent regulation of basal forebrain corticopetal neurons in attention: what exactly do telencephalic afferents “tell” basal forebrain neurons? 938 3.4. Arousal-induced attention and the role of basal forebrain noradrenergic afferents for the functional activation of telencephalic inputs to the basal forebrain 939 4. “AUTOSTIMULATION” OF BASAL FOREBRAIN CORTICOPETAL CHOLINERGIC NEURONS BY BRAINSTEM ASCENDING CHOLINERGIC PROJECTIONS MEDIATES DREAMING 942 4.1. Dreaming as hyperattentional processing 942 4.2. Increased cortical acetylcholine release and underlying afferent regulation in rapid eye movement sleep 943 4.3. Cortical cholinergic hyperactivity and hyperattentional processing 943 4.4. Cortical interactions between activated basal forebrain and thalamic projections in rapid eye movement sleep 945 4.5. Afferent regulation of basal forebrain and thalamic corticopetal neurons mediating dreaming cognition: implications for schizophrenia 945 5. CONCLUSIONS 946 ACKNOWLEDGEMENTS 946 REFERENCES 946 *To whom correspondence should be addressed. Fax: 11-614-688-4733. E-mail address: [email protected] (M. Sarter) Abbreviations: ACh, acetylcholine; AMPA, a-amino-3-hydroxy-5-methyl-4-isoxazolepropionate; AP5, 2-amino-5-phosphonopentanoic acid; BZR, benzo- diazepine receptor; CeA, central nucleus of the amygdala; DA, dopamine; EEG, electroencephalogram; LC, locus coeruleus; LDT, laterodorsal tegmental nucleus; mPFC, medial prefrontal cortex; NAC, nucleus accumbens; NMDA, N-methyl-d-aspartate; PPT, pedunculopontine tegmental nucleus; REM, rapid eye movement. 933 934 M. Sarter and J. P. Bruno 1. INTRODUCTION and of the psychopathological consequences of aberrations in the afferent regulation of these cortical input systems. Numerous recent experiments, using a variety of beha- vioral paradigms for the assessment of different aspects of attention, have concluded that the integrity of cortical cholin- 2. BEHAVIORAL AROUSAL AND ATTENTIONAL PERFORMANCE: ergic inputs is essential for the detection, selection and CONCEPTUAL OVERLAPS AND DIFFERENCES processing of stimuli and associations.36,52,146,179,216 Further- The attribution of “arousal” functions to basal forebrain more, basal forebrain neuropharmacological manipulations corticopetal neurons has been derived largely from neuro- known to increase or decrease the excitability of cortical pharmacological evidence supporting a “cholinergic nature” cholinergic inputs in intact rats bidirectionally alter the atten- of cortical arousal, specifically from studies showing relation- tional abilities of rats assessed in tasks designed to measure ships between electroencephalogram (EEG) desynchroniza- sustained or divided attention.94,184 Electrophysiological tion, increases in spontaneous alertness and increases in studies demonstrated that the increases in firing rate in medial cortical acetylcholine (ACh) turnover or cholinergic receptor prefrontal neurons accompanying increases in the demands on stimulation.34,166,201,209 These studies have further corrobor- sustained attention performance depend on the integrity of ated notions that the basal forebrain corticopetal system cholinergic inputs to this region.67 These and other data represents a rostral extension of the ascending reticular acti- support the hypothesis that cortical cholinergic inputs mediate vating system. Such notions have also been substantiated by diverse attentional functions, ranging from the ability to descriptions of the “reticular” anatomical and morphological detect and select stimuli that occur rarely and unpredictably characteristics of basal forebrain efferent projections, and by and require the subjects’ persistent readiness to detect such the innervation of the basal forebrain by projections originat- stimuli (as described by the theoretical construct “sustained ing in brainstem reticular areas.203 Presently, several inter- attention”), to discriminate significant stimuli from invalid related lines of evidence support the role of basal forebrain stimuli or “background noise” (“selective attention”), and to corticopetal projections in the regulation of “arousal”. Manip- allocate processing resources to competing demands on infor- ulations of the excitability of basal forebrain neurons mation processing (“divided attention”). Furthermore, aberra- modify cortical event-related potentials160 and other EEG tions in the integrity or excitability of basal forebrain measures.27,46,224 Likewise, neuronal activity in the basal fore- corticopetal cholinergic neurons have been described to escal- brain correlates with EEG activation.45,150,225 Furthermore, ate into major yet diverse cognitive dysfunctions and thus to basal forebrain neurons are involved in the diurnal regulation contribute essentially to the manifestation of the core cogni- of sleep parameters and associated EEG activity, probably tive symptoms of major neuropsychiatric disorders.181 due to connections with midbrain reticular and pontine struc- This rather recent literature on corticopetal cholinergic tures that represent the primary mediator of sleep–wake projections as a major component of the neuronal circuits rhythm9,107,207,211,212 (see below). Thus, the attribution of mediating attentional functions has rarely attempted to inte- “arousal”-like functions to basal forebrain corticopetal grate conceptually the more traditional descriptions of the projections has remained largely driven by research linking basal forebrain efferent system as a rostral extension of the the basal forebrain with brainstem ascending systems, and by ascending arousal system.1,95,136,210 Similar to Szymusiak’s210 studies assessing EEG and global behavioral states. discussion, the present review stresses the conceptual and A wide range of rather generally defined transitions from empirical overlaps, but also the differences, between the sleep or unconscious states to wakefulness, conscious aware- more traditional constructs of arousal and the more recent ness or the effective cortical processing of
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