Functional aspects of dopamine metabolism in the putative prefrontal cortex analogue and striatum of pigeons (Columba livia)

Dopamine (DA) in mammalian associative structures, such as the prefrontal cortex (PFC), plays a prominent role in learning and memory processes, and its homeostasis differs from that of DA in the striatum, a sensorimotor region. The neostriatum caudolaterale (NCL) of birds resembles the mammalian PFC according to connectional, electrophysiological, and behavioral data. In the present study, DA regulation in the associative NCL and the striatal lobus parolfactorius (LPO) of pigeons was compared to uncover possible differences corresponding to those between mammalian PFC and striatum. Extracellular levels of DA and its metabolites (homovanillic acid [HVA], dihydroxyphenylacetic acid [DOPAC]) and the serotonin metabolite 5‐hydroxyindoleacetic acid (5‐HIAA) were investigated by in vivo microdialysis of urethane‐anesthetized pigeons under basal conditions and after systemic administration of D‐amphetamine. DA was reliably determined only in LPO dialysates, and DA metabolite levels were significantly higher in LPO than in NCL. The HVA/DOPAC ratio, indicating extracellular lifetime of DA, was more than twice as high in NCL than in LPO dialysates. After amphetamine, DA increased in LPO while still being undetectable in NCL, and DA metabolites decreased in both regions. 5‐HIAA slightly decreased in NCL dialysates. Amphetamine effects were delayed in NCL compared with the striatum. In conclusion, effects of amphetamine on the pigeon's ascending monoamine systems resemble those found in mammals, suggesting similar regulatory properties. The neurochemical differences between NCL and LPO parallel those between associative regions, such as PFC and dorsal striatum in mammals. They may reflect weaker regulation of extracellular DA, favoring DAergic volume transmission, in associative than striatal forebrain regions. J. Comp. Neurol. 446:58–67, 2002. © 2002 Wiley‐Liss, Inc.

[1]  M. Koch,et al.  Impairment in a discrimination reversal task after D1 receptor blockade in the pigeon "prefrontal cortex". , 2000, Behavioral neuroscience.

[2]  Homan Hd,et al.  The effects of d-amphetamine and potassium on serotonin release and metabolism in rat cerebral cortex tissue. , 1981 .

[3]  P. Sanberg,et al.  The effect of striatal lesions in the chick on haloperidol-potentiated tonic immobility , 1983, Neuropharmacology.

[4]  K. Braun,et al.  N-methyl-D-aspartate receptor-mediated modulation of monoaminergic metabolites and amino acids in the chick forebrain: an in vivo microdialysis and electrophysiology study. , 1999, Journal of neurobiology.

[5]  E. Abercrombie,et al.  Differential Effect of Stress on In Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal Cortex , 1989, Journal of neurochemistry.

[6]  J. Barrett,et al.  Neurochemical changes correlated with behavior maintained under fixed-interval and fixed-ratio schedules of reinforcement. , 1991, Journal of the experimental analysis of behavior.

[7]  Lubica Kubikova,et al.  Influence of food restriction on dopamine receptor densities, catecholamine concentrations and dopamine turnover in chicken brain , 1999, Neuroscience.

[8]  Allan I. Levey,et al.  Dopamine Axon Varicosities in the Prelimbic Division of the Rat Prefrontal Cortex Exhibit Sparse Immunoreactivity for the Dopamine Transporter , 1998, The Journal of Neuroscience.

[9]  I. Divac,et al.  The prefrontal 'cortex' in the pigeon. Behavioral evidence. , 1982, Brain, behavior and evolution.

[10]  M. Herbin,et al.  Distribution of serotonin-immunoreactivity in the brain of the pigeon (Columba livia) , 1996, Anatomy and Embryology.

[11]  K. Hikosaka,et al.  Increase of extracellular dopamine in primate prefrontal cortex during a working memory task. , 1997, Journal of neurophysiology.

[12]  R. Roth,et al.  Characterization of dopamine release in the rat medial prefrontal cortex as assessed by in vivo microdialysis: Comparison to the striatum , 1990, Neuroscience.

[13]  M. Metzger,et al.  Organization of the dopaminergic innervation of forebrain areas relevant to learning: A combined immunohistochemical/retrograde tracing study in the domestic chick , 1996, The Journal of comparative neurology.

[14]  P. Goldman-Rakic,et al.  In vivo assessment of basal and drug‐induced dopamine release in cortical and subcortical regions of the anesthetized primate , 1993, Synapse.

[15]  E. Pehek,et al.  Comparison of effects of haloperidol administration on amphetamine-stimulated dopamine release in the rat medial prefrontal cortex and dorsal striatum. , 1999, The Journal of pharmacology and experimental therapeutics.

[16]  B. Jacobs,et al.  Dopaminergic input is required for increases in serotonin output produced by behavioral activation: an in vivo microdialysis study in rat forebrain , 1999, Neuroscience.

[17]  I. Divac,et al.  The prefrontal “cortex” in the pigeon catecholamine histofluorescence , 1985, Neuroscience.

[18]  J. Tanaka,et al.  Effects of discrimination learning on the rat amygdala dopamine release: a microdialysis study , 1993, Brain Research.

[19]  H. Niznik,et al.  The Dopamine D1D Receptor , 1995, The Journal of Biological Chemistry.

[20]  P. Garris,et al.  Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  G. Phillips,et al.  Enhanced dopamine efflux in the amygdala by a predictive, but not a non-predictive, stimulus: facilitation by prior repeated d-amphetamine , 1999, Neuroscience.

[22]  H. D. Homan,et al.  The effects of d-amphetamine and potassium on serotonin release and metabolism in rat cerebral cortex tissue. , 1981, Research communications in chemical pathology and pharmacology.

[23]  J. Fuster Prefrontal Cortex , 2018 .

[24]  J. P. Huston,et al.  The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments , 1996, Progress in Neurobiology.

[25]  I. Divac,et al.  Dopaminergic innervation of the brain in pigeons. The presumed 'prefrontal cortex'. , 1994, Acta neurobiologiae experimentalis.

[26]  Susan R. George,et al.  Cloning of the gene for a human dopamine D5 receptor with higher affinity for dopamine than D1 , 1991, Nature.

[27]  D. McMillan,et al.  Effects ofd-amphetamine on spontaneous motor activity in pigeons , 2004, Psychopharmacology.

[28]  J. Carlson,et al.  Estimating Extracellular Concentrations of Dopamine and 3,4‐Dihydroxyphenylacetic Acid in Nucleus Accumbens and Striatum Using Microdialysis: Relationships Between In Vitro and In Vivo Recoveries , 1994, Journal of neurochemistry.

[29]  Onur Gu¨ntu¨rku¨n,et al.  The dopaminergic innervation of the pigeon caudolateral forebrain: immunocytochemical evidence for a ‘prefrontal cortex’ in birds? , 1993, Brain Research.

[30]  A. Reiner,et al.  Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. , 1995, Brain, behavior and evolution.

[31]  K. Braun,et al.  Distinct activation of monoaminergic pathways in chick brain in relation to auditory imprinting and stressful situations: a microdialysis study , 1996, Neuroscience.

[32]  L S Seiden,et al.  Amphetamine: effects on catecholamine systems and behavior. , 1993, Annual review of pharmacology and toxicology.

[33]  G. Phillips,et al.  Repeated d-amphetamine enhances stimulated mesoamygdaloid dopamine transmission , 1997, Psychopharmacology.

[34]  Reinhild Schnabel,et al.  The dorsocaudal neostriatum of the domestic chick: a structure serving higher associative functions , 1999, Behavioural Brain Research.

[35]  R. Schwarting,et al.  Dopamine and Serotonin Metabolism in Brain Sites Ipsi‐ and Contralateral to Direction of Conditioned Turning in Rats , 1987, Journal of neurochemistry.

[36]  G. Striedter,et al.  The “Neostriatum” Develops as Part of the Lateral Pallium in Birds , 1998, The Journal of Neuroscience.

[37]  O. Güntürkün,et al.  Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons: Possible behavioral equivalencies to the mammalian prefrontal system , 1998, Behavioural Brain Research.

[38]  O. Güntürkün Cognitive impairments after lesions of the neostriatum caudolaterale and its thalamic afferent in pigeons: functional similarities to the mammalian prefrontal system? , 1997, Journal fur Hirnforschung.

[39]  G. Arbuthnott,et al.  Amphetamine‐Induced Dopamine Release in the Rat Striatum: An In Vivo Microdialysis Study , 1988, Journal of neurochemistry.

[40]  G. Nisticó,et al.  Dopaminergic mechanisms and stereotyped behaviour in birds. , 1979, Pharmacological research communications.

[41]  I. Goodman Amphetamine and apomorphine induced stereotyped behavior in adult pigeons , 1981, Pharmacology Biochemistry and Behavior.

[42]  J E LeDoux,et al.  Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations. , 1999, Behavioral neuroscience.

[43]  R. Roth,et al.  Dopamine Synthesis, Uptake, Metabolism, and Receptors: Relevance to Gene Therapy of Parkinson's Disease , 1997, Experimental Neurology.

[44]  D. Durstewitz,et al.  The dopaminergic innervation of the pigeon telencephalon: distribution of DARPP-32 and co-occurrence with glutamate decarboxylase and tyrosine hydroxylase , 1998, Neuroscience.

[45]  M. Vogt,et al.  Monoamines and their metabolites in the avian brain , 1967, The Journal of physiology.

[46]  O. Güntürkün,et al.  Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): A retro‐ and anterograde pathway tracing study , 1999, The Journal of comparative neurology.

[47]  D. Durstewitz,et al.  The dopaminergic innervation of the avian telencephalon , 1999, Progress in Neurobiology.

[48]  I. Divac,et al.  Behavioural effects of ablation of the pigeon-equivalent of the mammalian prefrontal cortex , 1993, Behavioural Brain Research.

[49]  T. Robbins,et al.  Chemical neuromodulation of frontal-executive functions in humans and other animals , 2000, Experimental Brain Research.

[50]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[51]  O. Güntürkün,et al.  Single unit activity during a Go/NoGo task in the “prefrontal cortex” of pigeons , 1999, Brain Research.

[52]  R. Schwarting,et al.  Relationship between dopamine release in nucleus accumbens and place preference induced by substance P injected into the nucleus basalis magnocellularis region , 1995, Neuroscience.

[53]  G. Gerhardt,et al.  In Vivo Assessment of Dopamine Uptake in Rat Medial Prefrontal Cortex: Comparison with Dorsal Striatum and Nucleus Accumbens , 1995, Journal of neurochemistry.

[54]  M. Raiteri,et al.  d-Amphetamine as a releaser or reuptake inhibitor of biogenic amines in synaptosomes. , 1975, European journal of pharmacology.

[55]  D. Segal,et al.  Concomitant characterization of behavioral and striatal neurotransmitter response to amphetamine using in vivo microdialysis , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  R. Wightman,et al.  Mechanisms of Amphetamine Action Revealed in Mice Lacking the Dopamine Transporter , 1998, The Journal of Neuroscience.

[57]  O. Güntürkün,et al.  Dopaminergic innervation of the telencephalon of the pigeon (Columba livia): A study with antibodies against tyrosine hydroxylase and dopamine , 1995, The Journal of comparative neurology.

[58]  Charles L. Wilson,et al.  Increased dopamine release in the human amygdala during performance of cognitive tasks , 2001, Nature Neuroscience.

[59]  D. Davies,et al.  Distribution of CGRP‐like immunoreactivity in the chick and quail brain , 2000, The Journal of comparative neurology.

[60]  U. Ungerstedt,et al.  In Vivo Measurement of Dopamine and Its Metabolites by Intracerebral Dialysis: Changes After d‐Amphetamine , 1983, Journal of neurochemistry.

[61]  J. Rubenstein,et al.  Comparison of the mammalian and avian telencephalon from the perspective of gene expression data. , 1999, European journal of morphology.

[62]  I. Divac,et al.  The Prefrontal 'Cortex' in the Pigeon , 1982 .

[63]  G. Gerhardt,et al.  Microdialysis studies of basal levels and stimulus-evoked overflow of dopamine and metabolites in the striatum of young and aged Fischer 344 rats , 1999, Brain Research.

[64]  P. Greengard,et al.  Localization of dopamine D1 receptors and dopaminoceptive neurons in the chick forebrain , 1997, The Journal of comparative neurology.

[65]  T. Sejnowski,et al.  The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms. , 1994, Learning & memory.

[66]  U. Ungerstedt,et al.  An In Vivo Study of Dopamine Release and Metabolism in Rat Brain Regions Using Intracerebral Dialysis , 1986, Journal of neurochemistry.

[67]  R. Wightman,et al.  Re-evaluation of the role of the dopamine transporter in dopamine system homeostasis 1 Published on the World Wide Web on 27 January 1998. 1 , 1998, Brain Research Reviews.

[68]  R. Wightman,et al.  Profound neuronal plasticity in response to inactivation of the dopamine transporter. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[69]  F. Artigas,et al.  Regional Distribution of Extracellular 5‐Hydroxytryptamine and 5‐Hydroxyindoleacetic Acid in the Brain of Freely Moving Rats , 1991, Journal of neurochemistry.

[70]  W. Bock THE ORIGIN AND RADIATION OF BIRDS * , 1969 .

[71]  S. D. Glick,et al.  Similar effects ofd-amphetamine and cocaine on extracellular dopamine levels in medial prefrontal cortex of rats , 1990, Brain Research.

[72]  D. Pelligrino,et al.  Cyclic nucleotide crosstalk and the regulation of cerebral vasodilation , 1998, Progress in Neurobiology.

[73]  Luigi F. Agnati,et al.  The emergence of the volume transmission concept 1 Published on the World Wide Web on 12 January 1998. 1 , 1998, Brain Research Reviews.

[74]  P. Goldman-Rakic,et al.  D1 dopamine receptors in prefrontal cortex: involvement in working memory , 1991, Science.