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In Viva Comparison of the Regulation of Releasable Dopamine in the Caudate Nucleus and the Nucleus Accumbens of the Rat Brain

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In Viva Comparison of the Regulation of Releasable Dopamine in the Caudate Nucleus and the Nucleus Accumbens of the Rat Brain The Journal of Neuroscience April 1986, 6(4): 974-982 In viva Comparison of the Regulation of Releasable Dopamine in the Caudate Nucleus and the Nucleus Accumbens of the Rat Brain Werner G. Kuhr, James C. Bigelow, and Ft. Mark Wightman Department of Chemistry, Indiana University, Bloomington, Indiana 47405 In viva voltammetry has been used to measure the release of do- ognized major difference of these two brain regions is the func- pamine evoked by electrical stimulation of the medial forebrain tion of neuronal feedback loops for the two pathways. The stria- bundle (MFB). Simultaneous measurements have been made tonigral pathway (Javoy et al., 1972) plays a large regulatory with voltammetric-sensing electrodes ipsilateral to the stimulat- role, while considerable evidence exists that a corresponding ing electrode in the nucelus accumbens and the caudate nucleus regulation does not exist for the nucleus accumbens (Wang, of the anesthetized rat. During the stimulation, the species ob- 198 la, b). However, it is less clear whether different local factors served in both regions is voltammetrically identical to dopa- exist that regulate dopamine release in these two brain regions. mine. Further evidence for the identity of dopamine is provided Electrical stimulation of the medial forebrain bundle (MFB) by anatomical, physiological, pharmacological, and postmortem has been used extensively to activate dopamine neurons for data. Postmortem analysis of these brain regions after a single studying behavior mediated by dopamine, or for examining stimulation demonstrates that dopamine levels are unchanged, changes in levels of dopamine or its metabolites (for a review, while dihydroxyphenylacetic acid (DOPAC) levels are in- see Korf, 1979). We have previously shown that stimulation of creased in both regions. Systemic application of synthesis in- this neuronal tract causes a release of dopamine that can be hibitors results in a decrease in evoked release for each brain monitored with a carbon fiber voltammetric electrode implanted region. Amfonelic acid results in a restoration of stimulated re- at the caudate nucleus (Ewing and Wightman, 1984; Ewing et lease after synthesis inhibition. Evoked release is affected dif- al., 1983; Kuhr et al., 1984). Dopamine has been identified as ferently by pargyline in the two brain regions. The evoked re- the compound detected in the caudate nucleus by voltammetric, lease of dopamine is significantly elevated in the nucleus anatomical, physiological, pharmacological, and postmortem accumbens as a result of pargyline administration, but similar data. The dopamine that is observed in the extracellular fluid effects are not seen in the caudate nucleus. Tissue levels of do- of the caudate nucleus as a result of evoked release is related to pamine are increased in both brain regions by pargyline, but the amount of dopamine in the releasable pool (Ewing et al., the increase is significantly greater in the accumbens. Electro- 1983). For example, synthesis inhibition results in a decrease lytic lesions of the striatonigral pathway or systemic adminis- of dopamine observed during stimulation, while enhancement tration of picrotoxin eliminates the pargyline-induced difference of dopamine synthesis has an opposite effect (Stamford et al., in evoked release of dopamine. Amphetamine causes a reduction 1985). Thus, the combination of in vivo voltammetry, which en- in stimulated release in the caudate nucleus with little effect on ables identification of dopamine, with electrical stimulation of that observed in the nucleus accumbens. Administration of par- neuronal processesprovides an ideal way to examine the factors gyline prior to amphetamine results in a diminution of release that affect the dopamine releasable pool. in both brain regions. Taken together, these data indicate that In this work, we present data that demonstrate the similarities different factors affect regulation of the releasable pool of do- and differences of the evoked release of dopamine in the caudate pamine in the nucleus accumbens and caudate nucleus. nucleus and nucleus accumbens following electrical stimulation of the MFB. Evidence will be presented that establishes that Several major dopaminergic systems exist in the mammalian dopamine is the major substance detected in the nucleus ac- brain, including the nigrostriatal and mesolimbic systems. It is cumbens. As will be shown, evoked release of dopamine suggests known that the mesolimbic system plays an important role in that the functional stores of this neurotransmitter are regulated the regulation of normal brain function, and this role is distinct in different ways in the two brain regions. A major difference from that played by the nigrostriatal dopamine pathway (Mo- in regulation will be shown to occur via monoamine oxidase genson and Yin, 1981; White and Wang, 1982). It has been (MAO). shown by unit-recording techniques that these two regions re- spond in different manners to pharmacological stimuli thought Materials and Methods to affect dopaminergic neurons (Rebec and Zimmerman, 1980; Reynolds et al., 1981). The behavioral responses elicited by Stimulated dopamine release electrical stimulation of these two pathways differ (van der Hey- The surgicalprocedure, stimulation parameters,and electrodesand ap- den, 1984). Lesions of the two regions also produce different paratus have been describedin detail in a previous publication (Kuhr behavioral responses (Kelly and Moore, 1976; Pycock and et al., 1984).Male Sprague-Dawleyrats were anesthetizedwith chloral Marsden, 1978). Furthermore, anatomical differences have been hydrate and placed in a stereotaxicframe. Disk-shapedelectrodes (di- shown at an ultrastructural level (Bouyer et al., 1984). A rec- ameter = 12 pm) were fabricated from carbon fibers sealedin glass capillary tubes.Two of thesemicrovoltammetric electrodes, mounted on ReceivedJune 10, 1985;revised Oct. 7, 1985;accepted Oct. 10, 1985. the same stereotaxic holder, were lowered into the caudatenucleus and This work was supportedby a grant from the National ScienceFoundation, nucleus accumbens at the following stereotaxic coordinates: AP, 3.5, NeurobiologySection. 2.5; L, 1.5; V, -6.2, -4.0 mm, as measuredfrom bregmaand dura Correspondenceshould be addressedto R. M. Wigbtman,Department ofChem- (Pelligrino and Cushmann, 1967). Placement was verified by histology. istry, Indiana University, Bloomington,IN 47405. The electrodeswere connectedto a multielectrode potentiostat. Data Copyright 0 1986Society for Neuroscience0270-6474/86/040974-09$02.00/O acquisition and control were handled by a microcomputer(Ewing et al., The Journal of Neuroscience MAO Regulation of Releasable DA in Rat Caudate and Accumbens 975 Figure I. Response of a microvolt- ammetric disk electrode placed in the nucleus accumbens to a 10 set, 60 Hz, 80 PA sinusoidal stimulation of the MFB. Time-course data were ob- tained with repetitive chronoamper- ometry (92 msec pulse, -0.2 to 0.5 V vs standard calomel electrode (SCE), repeated every 2 set). Insert, Sub- tracted normal pulse voltammograms obtained in vivo at the peak of stim- ulation (solid line) and in vitro follow- ing the in vivo experiment (squares, 40 PM DA, circles, 200 PM AA, tri- UngkS, 40 pM DOPAC). SCanS Were obtained every 4 set (-0.2 to +0.5 V vs SCE, 250 mV/sec); the in vivo re- sult was obtained by subtraction of a -IV u IV zu 3u 4u scanbefore the stimulation from a scan TIME (Seconds) at the peak of stimulation. 1982). Voltammograms were obtained with normal pulse, backstep- corrected voltammetry (Ewing et al., 198 1). This technique has been pre- Electrolytic lesions viously shown to give distinct voltammograms for catecholamines (Ko- Lesions of the crus cerebri were made in chloral hydrate anesthetized vach et al., 1984). However, the techique is not sufficiently sensitive to animals by placing a bipolar-stimulating electrode (Plastic Products; tip detect the basal concentration of catecholamines in extracellular fluid spacing 0.64 mm)at the stereotaxic coordinates (relative to bregma and (Ewing et al., 1982, 1983). dura) AP. 4.1: L. 2.4: and V. -9.0 (during lesions, the upper incisor A bipolar-stimulating electrode (Plastic Products Co., Roanoke, VA, bar was placed at thelevel of the interaurai line). A 2 mA-DC current tip spacing equals 0.65 mm) was used to stimulate the MFB. The stim- was passed for 15 set at constant current, using a Grass Model DC- ulating electrode was placed 2.2 mm posterior to bregma and 1.6 mm LM5 lesion maker (Grass Instruments, Quincy, MA). Animals were lateral to the central suture. Location of the MFB was accomplished as allowed to recuperate for one week prior to experimentation. Lesions previously described, and the placement of the tip of the stimulating were verified histologically after in vivo experimentation. Postmortem electrode was adjusted for maximal response in each region (Kuhr et analvsis of lesioned animals showed increased levels of DOPAC and al., 1984). Except as noted, stimulations consisted of sinusoidal 60 Hz. HVA in the striatum, with no change in dopamine levels, in agreement 80 PA rms current applied for 10 set at 20 min intervals. with previous reports (Di Chiara et al., 1977). Postmortem tissue analysis Monoamine oxidase assay Rats were killed and their brains were quickly removed and placed in MAO B activity was assayed, using a modification of Nissinen’s (1984) ice-cold saline. The nucleus accumbens was dissected according to the procedure. For each assay, striatal or accumbens
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