Dopaminergic regulation of feeding behavior: II. Differential effects of amphetamine microinfusion into three striatal subregions

In the present study, the role of dopaminergic mechanisms within different striatal subregions in feeding behavior was examined in food-deprived (19 h) rats. Specifically, the dopamine (DA) antagonist haloperidol (0, 0.025, 0.25, 2.5 μg/0.5 μl) was infused bilaterally into the nucleus accumbens (N.Acc), the ventrolateral striatum (VLS), or the dorsolateral striatum (DLS), and a microanalysis of ingestive behavior and spontaneous motor behavior was carried out. When infused into the N. Ace, haloperidol increased feeding duration, food intake, and the average duration of a feeding bout. Locomotor activity and drinking behavior were reduced by N.Acc. haloperidol infusion. In contrast, feeding was attenuated when haloperidol was infused into the VLS. Drinking and locomotion were unaffected. Few changes in ingestive behavior were noted following DA-antagonist treatment of the dorsolateral site. It is hypothesized that DA transmission in the N.Acc. normally facilitates switching between different competing behaviors, that the VLS is critical for control of oral motor mechanisms, and that the DLS is minimally involved in modulating ingestive behavior.

[1]  P. Willner,et al.  The Mesolimbic Dopamine System: From Motivation to Action An International Workshop Malta September 25–29, 1989 , 1989, Psychobiology.

[2]  S. Iversen.  Brain Dopamine Systems and Behavior , 1977 .

[3]  P. Teitelbaum,et al.  The lateral hypothalamic syndrome: recovery of feeding and drinking after lateral hypothalamic lesions. , 1962, Psychological review.

[4]  P. Sawchenko,et al.  Paraventricular area: Critical focus of a longitudinal neurocircuitry mediating food intake , 1977, Physiology & Behavior.

[5]  A. Ettenberg,et al.  Haloperidol induces a partial reinforcement extinction effect in rats: Implications for a dopamine involvement in food reward , 1986, Pharmacology Biochemistry and Behavior.

[6]  A. E. Fisher,et al.  Tail pinch-induced eating, gnawing and licking behavior in rats: Dependence on the nigrostriatal dopamine system , 1975, Brain Research.

[7]  R. Wise,et al.  Neuroleptic-induced "anhedonia" in rats: pimozide blocks reward quality of food. , 1978, Science.

[8]  E. Valenstein,et al.  The propensity for nonregulatory ingestive behavior is related to differences in dopamine systems: behavioral and biochemical evidence. , 1986, Behavioral neuroscience.

[9]  J. Joyce,et al.  Rotation and postural deviation elicited by microinjections of dopamine into medial and lateral regions of dorsal striatum , 1984, Pharmacology Biochemistry and Behavior.

[10]  A. Kelley,et al.  Amphetamine microinjections into distinct striatal subregions cause dissociable effects on motor and ingestive behavior , 1989, Behavioural Brain Research.

[11]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[12]  D. Bindra.  Neuropsychological interpretation of the effects of drive and incentive-motivation on general activity and instrumental behavior. , 1968 .

[13]  S. Hanson,et al.  Arousal: its genesis and manifestation as response rate. , 1978, Psychological review.

[14]  J. Blundell.  Structure, Process, and Mechanism: Case Studies in the Psychopharmacology of Feeding , 1987 .

[15]  A. Phillips,et al.  Haloperidol-induced disruption of conditioned avoidance responding: attenuation by prior training or by anticholinergic drugs. , 1975, European journal of pharmacology.

[16]  R. Bolles.  Reinforcement, expectancy, and learning. , 1972 .

[17]  S. W. Ranson,et al.  Experimental Hypothalamico-Hypophyseal Obesity in the Rat.∗ , 1939 .

[18]  J. Salamone.  Dopaminergic involvement in activational aspects of motivation: Effects of haloperidol on schedule-induced activity, feeding, and foraging in rats , 1988, Psychobiology.

[19]  S. Iversen,et al.  Handbook of Psychopharmacology , 1988, Springer US.

[20]  M. Zigmond,et al.  Effects of dopaminergic agonists and antagonists of feeding in intact and 6-hydroxydopamine-treated rats. , 1977, The Journal of pharmacology and experimental therapeutics.

[21]  T. Robbins,et al.  Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. , 1978, Journal of comparative and physiological psychology.

[22]  M. Pisa,et al.  Dissociable motor roles of the rat's striatum conform to a somatotopic model. , 1988, Behavioral neuroscience.

[23]  R. Beninger.  The role of dopamine in locomotor activity and learning , 1983, Brain Research Reviews.

[24]  G. Mogenson,et al.  Neuropharmacological and electrophysiological evidence implicating the mesolimbic dopamine system in feeding responses elicited by electrical stimulation of the medial forebrain bundle , 1982, Brain Research.

[25]  A. Phillips,et al.  Dopamine and preparatory behavior: I. Effects of pimozide. , 1987, Behavioral neuroscience.

[26]  L. Pellegrino,et al.  stereotaxic atlas of the rat brain , 1967 .

[27]  A. Ettenberg.  Dopamine, neuroleptics and reinforced behavior , 1989, Neuroscience & Biobehavioral Reviews.

[28]  H. Anisman,et al.  Alteration of exploration and the response to food associated cues after treatment with pimozide , 1983, Pharmacology Biochemistry and Behavior.

[29]  J. Marshall,et al.  Dopamine in the lateral caudate-putamen of the rat is essential for somatosensory orientation. , 1986, Behavioral neuroscience.

[30]  R. Beninger.  A comparison of the effects of pimozide and nonreinforcement on discriminated operant responding in rats , 1982, Pharmacology Biochemistry and Behavior.

[31]  M. Zigmond,et al.  The effect of altered dopaminergic activity on food intake in the rat: evidence for an optimal level of dopaminergic activity for behavior. , 1980, Progress in neuro-psychopharmacology.

[32]  P. Rogers,et al.  Effects of anorexie drugs on food intake, food selection and preferences and hunger motivation and subjective experiences , 1980, Appetite.

[33]  A. Phillips,et al.  Increased dopamine metabolism in the nucleus accumbens and striatum following consumption of a nutritive meal but not a palatable non-nutritive saccharin solution , 1986, Pharmacology Biochemistry and Behavior.

[34]  T. Robbins,et al.  Stress-induced eating: Fact, fiction or misunderstanding? , 1980, Appetite.

[35]  R G Robinson,et al.  Measurement of appetite disturbances in psychiatric disorders. , 1975, Journal of psychiatric research.

[36]  A. Phillips,et al.  Dopamine and preparatory behavior: II. A neurochemical analysis. , 1989 .

[37]  R. M. Beckstead.  An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat , 1979, The Journal of comparative neurology.

[38]  H. Szechtman,et al.  Tail pinch induces eating in sated rats which appears to depend on nigrostriatal dopamine. , 1975, Science.

[39]  P. Kalivas,et al.  The mesocorticolimbic dopamine system. , 1988, Annals of the New York Academy of Sciences.

[40]  T. Heffner,et al.  Feeding increases dopamine metabolism in the rat brain. , 1980, Science.

[41]  R. Wise,et al.  Concurrent facilitory and inhibitory effects of amphetamine on stimulation-induced eating , 1988, Brain Research.

[42]  A. Kelley,et al.  The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: An anterograde and retrograde-horseradish peroxidase study , 1982, Neuroscience.

[43]  I. Whishaw,et al.  “Stick out your tongue”: Tongue protrusion in neocortex and hypothalamic damaged rats , 1983, Physiology & Behavior.

[44]  G. Koob,et al.  Hyperactivity and hypoactivity produced by lesions to the mesolimbic dopamine system , 1981, Behavioural Brain Research.

[45]  A. E. Fisher,et al.  Stimulation bound ingestive behavior: A view from the tail , 1976, Physiology & Behavior.

[46]  R. M. Gold.  Hypothalamic Obesity: The Myth of the Ventromedial Nucleus , 1973, Science.

[47]  K. Berridge,et al.  Taste reactivity analysis of 6-hydroxydopamine-induced aphagia: implications for arousal and anhedonia hypotheses of dopamine function. , 1989, Behavioral neuroscience.

[48]  F. Vaccarino,et al.  Intra-nucleus accumbens amphetamine: Dose-dependent effects on food intake , 1986, Pharmacology Biochemistry and Behavior.

[49]  N. White,et al.  Contributions of dopamine terminal areas to amphetamine-induced anorexia and adipsia , 1986, Pharmacology Biochemistry and Behavior.

[50]  S. Leibowitz.  Amphetamine: possible site and mode of action for producing anorexia in the rat , 1975, Brain Research.

[51]  T. Robbins,et al.  Selective disruption of displacement behaviour by lesions of the mesolimbic dopamine system , 1980, Nature.

[52]  S. Iversen,et al.  Regulatory impairments following selective 6-OHDA lesions of the neostriatum , 1982, Behavioural Brain Research.

[53]  J. Marshall,et al.  Neostriatal dopamine and sensory inattention. , 1980, Journal of comparative and physiological psychology.

[54]  V. Bakshi,et al.  Dopaminergic regulation of feeding behavior: I. Differential effects of haloperidol microinfusion into three striatal subregions , 1991, Psychobiology.

[55]  J. Salamone,et al.  Characterization of the impaired feeding behavior in rats given haloperidol or dopamine-depleting brain lesions , 1990, Neuroscience.

[56]  I. Whishaw,et al.  The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. , 1986, Brain : a journal of neurology.

[57]  F. S. Radhakishun,et al.  Scheduled eating increases dopamine release in the nucleus accumbens of food-deprived rats as assessed with on-line brain dialysis , 1988, Neuroscience Letters.

[58]  P. Teitelbaum,et al.  Nigrostriatal bundle damage and the lateral hypothalamic syndrome. , 1974, Journal of comparative and physiological psychology.

[59]  W. Nauta,et al.  The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods , 1982, Neuroscience.

[60]  S. Leibowitz,et al.  Amphetamine: Effects on meal patterns and macronutrient selection , 1986, Brain Research Bulletin.

[61]  U. Ungerstedt.  Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. , 1971, Acta physiologica Scandinavica. Supplementum.

[62]  F. Vaccarino,et al.  Amphetamine- and morphine-induced feeding: Evidence for involvement of reward mechanisms , 1990, Neuroscience & Biobehavioral Reviews.

[63]  R. Wise,et al.  Facilitory and Inhibitory Effects of Nucleus Accumbens Amphetamine on Feeding , 1988 .

[64]  R. Roth,et al.  Telencephalic Projections of the A8 Dopamine Cell Group , 1988, Annals of the New York Academy of Sciences.

[65]  M. Pisa.  Motor functions of the striatum in the rat: Critical role of the lateral region in tongue and forelimb reaching , 1988, Neuroscience.

[66]  R. Wise.  Neuroleptics and operant behavior: The anhedonia hypothesis , 1982, Behavioral and Brain Sciences.

[67]  James L Olds,et al.  Effects of chlorpromazine, meprobamate, pentobarbital and morphine on self-stimulation. , 1960, The Journal of pharmacology and experimental therapeutics.

[68]  I. Stolerman.  Eating, drinking and spontaneous activity in rats after the administration of chlorpromazine. , 1970, Neuropharmacology.

[69]  J. Brobeck,et al.  Hypothalamic Control of Food Intake in Rats and Cats * , 1951, The Yale journal of biology and medicine.

[70]  J. B. Justice,et al.  Dopamine depletion in a striatal subregion disrupts performance of a skilled motor task in the rat , 1985, Brain Research.

[71]  J. Stellar,et al.  The Neurobiology of Motivation and Reward , 1985 .

[72]  J. Blundell,et al.  Characterisation of adjustments to the structure of feeding behaviour following pharmacological treatment: Effects of amphetamine and fenfluramine and the antagonism produced by pimozide and methergoline , 1980, Pharmacology Biochemistry and Behavior.

[73]  Aaron Ettenberg,et al.  Haloperidol blocks the response-reinstating effects of food reward: A methodology for separating neuroleptic effects on reinforcement and motor processes , 1988, Pharmacology Biochemistry and Behavior.

[74]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[75]  N. Geary,et al.  Pimozide decreases the positive reinforcing effect of sham fed sucrose in the rat , 1985, Pharmacology Biochemistry and Behavior.