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NEUROPHARMACOLOGY
Department of Pharmacology and Toxicology, University of Utah, Salt Lake City, Utah (K.A.H., G.R.H., K.A.K.); and Westar Corporation/Dugway Engineering, Dugway, Utah (S.C.W.)
Received April 25, 2006; accepted July 11, 2006.
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Abstract |
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; Hotchkiss and Gibb, 1980; Wilson et al., 1996; Volkow et al., 2001). In particular, repeated high doses of METH can lead to loss of monoaminergic input to the striatum as well as cell death in the striatum (Kogan et al., 1976; Hotchkiss and Gibb, 1980; Deng et al., 1999, 2002; Cadet et al., 2003).
The striatum consists of two main cell types: medium spiny projection neurons and aspiny interneurons. Projection neurons are GABA-positive neurons that also express the neuropeptides substance P (SP), dynorphin, enkephalin, or neurotensin (Gerfen and Wilson, 1996; Kawaguchi, 1997). Striatal interneurons, in contrast, are either cholinergic, parvalbumin/GABAergic, calretinin/GABAergic, or neuronal nitric-oxide synthase (nNOS)/somatostatin (SOM)/neuropeptide Y (NPY)-positive (Vincent et al., 1983; Kubota et al., 1988; Kawaguchi et al., 1995). Several studies have shown that NPY/nNOS-positive interneurons may be resistant to neurotoxic processes. For example, NPY-positive, but not enkephalin-positive, neurons are not damaged by quinolinic acid-induced lesions in the striatum (Koh et al., 1986; Beal et al., 1991; Mitchell et al., 1999) and nNOS/NPY-positive neurons are spared after a multiple dosing regimen of METH that induced apoptosis of enkephalin-positive neurons in the mouse striatum (Thiriet et al., 2005). Furthermore, recent work suggests that NPY itself may act as a neuroprotective agent, because administration of NPY or NPY receptor agonists blocked METH-induced cell death in mouse striatum (Thiriet et al., 2005). In line with this hypothesis is the observation that neurotoxic doses of METH reduce tissue levels of NPY in the striatum, indicating that there may be an increase in NPY release by interneurons in the striatum in response to this dosing regimen (Westwood and Hanson, 1999). Together, these data suggest that a neurotoxic insult (such as the multiple METH dosing regimen) may activate the NPY system in the striatum, possibly as a protective response to potential neurotoxic injury.
Although previous work has examined METH-induced changes in tissue levels of NPY in the striatum (Westwood and Hanson, 1999), few studies have addressed the possible changes in NPY mRNA expression in the interneuron population in the striatum in response to a neurotoxic regimen of METH treatment. Recently, Thiriet et al. (2005) used quantitative real-time-PCR to demonstrate that a neurotoxic regimen of METH treatment increased NPY mRNA in mouse striatum (Thiriet et al., 2005). However, this study gives little information on the anatomical changes in NPY mRNA expression in the interneuron population of the striatum that may occur after a neurotoxic regimen of METH, as well as the pharmacology underlying this effect.
Thus, the purpose of the present study was to examine the effects of a toxic dosing regimen of METH (Kogan et al., 1976) on ppNPY mRNA expression in the striatum. Since our previous work has shown that blockade of DA D1 receptors attenuates the reduction in NPY-like immunoreactivity in the striatum induced by a toxic dosing regimen of METH (Westwood and Hanson, 1999), we investigated the effects of DA D1 and D2 receptor blockade on multiple METH-induced changes in NPY mRNA expression. We also examined changes in pSOM mRNA expression in the striatum in response to multiple METH treatment and DA receptor blockade, because somatostatin is coexpressed with NPY in striatal interneurons.
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Materials and Methods |
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(±)-Methamphetamine hydrochloride was obtained from the National Institute on Drug Abuse (Bethesda, MD). SCH23390 and eticlopride were obtained from Sigma-Aldrich (St. Louis, MO). All drugs were calculated as the free base, dissolved in saline, and administered in a volume of 1 ml/kg. All injections were given intraperitoneally.
On the day of the experiment, the rats were weighed, housed in plastic tub cages with sawdust bedding (four rats per cage), and transferred to the laboratory. Animals were given five injections of 10 mg/kg METH at 6-h intervals. Control animals received multiple injections of saline. This METH-dosing regimen has previously been shown to significantly reduce dopamine levels and tyrosine hydroxylase activity in the striatum (Kogan et al., 1976). Animals were sacrificed 3 h after the last injection. In a subset of experiments, 0.5 mg/kg eticlopride, 0.5 mg/kg SCH23390, or saline was administered 15 min before each METH injection. In a separate experiment, animals were given a single, high dose of METH (15 mg/kg), and they were sacrificed 3 h after treatment.
Rats were sacrificed by exposure to CO2 for 1 min, followed by decapitation. The brains were rapidly harvested and quick-frozen in isopentane on dry ice. Brains were stored at -20°C until they were cut into 12-µm sections on a cryostat (Cryocut 1800; Cambridge Instruments, Bayreuth, Germany). Sections were thaw mounted on slides and stored at -20°C. Slides from all animals were then post-fixed in 4% paraformaldehyde/0.9% sodium chloride; acetylated in fresh 0.25% acetic anhydride in 0.1 M triethanolamine/0.9% sodium chloride, pH 8.0; dehydrated in alcohol; delipidated in chloroform; and gradually rehydrated in a descending series of alcohol concentrations. Slides were air-dried and stored at -20°C.
For detection of pSOM mRNA, a 39-base oligonucleotide probe was used that was complementary to bases 1 to 39 of the 3' coding region of the pSOM gene (Fitzpatrick-McElligott et al., 1988). The probe was synthesized by the DNA/peptide facility at the University of Utah (Salt Lake City, UT) and end labeled using terminal deoxynucleotidyl transferase (Roche Biomedical Laboratories) and 35S-dATP (PerkinElmer NEN). The probe was diluted in hybridization buffer [0.6 M sodium chloride, 80 mM Tris, 4 mM EDTA, 0.1% (w/v) sodium pyrophosphate, 10% (w/v) dextran, 0.2% (w/v) lauryl sulfate, 0.5 mg/ml heparin, and 50% formamide], and 90 µl of the probe in hybridization buffer was applied to each slide and covered with glass coverslips. Slides were hybridized overnight in humid chambers at 37°C. The slides were then washed four times in 1x SSC (0.15 M sodium chloride and 0.015 M sodium citrate, pH 7.2) at room temperature and then three times in 20 min in 2x SSC with 50% (v/v) formamide at 42°C. Slides were washed two times each for 30 min (for 60 min total) in 1x SSC at room temperature, rinsed briefly in deionized water, and air-dried.
For the detection of ppNPY mRNA, a full-length ribonucleotide probe (Larhammar et al., 1987) was synthesized from the cDNA using 35S-UTP (PerkinElmer Life and Analytical Sciences, Boston, MA) and T7 RNA polymerase (Roche Biomedical Laboratories, Burlington, NC). The probe was mixed with nuclease-free water and RNA mix (final concentrations): 100 µg/µl salmon sperm DNA, 250 µg/µl yeast total RNA, and 250 µg/µl tRNA). The solution was heated at 65°C for 5 min and cooled on ice for 1 min. The following compounds were added to the solution (final concentrations): 100 mM dithiothreitol, 0.2% (w/v) sodium dodecyl sulfate, 0.11% (w/v) sodium thiosulfate, and hybridization buffer [23.8 mM Tris, pH 7.4, 1.2 mM EDTA, pH 8.0, 357 mM NaCl, 11.9% (w/v) dextran, 1.2x Denhardt's solution, and 59.5% (w/v) formamide] to the appropriate dilution. Hybridization buffer containing probe (2 x 106 cpm/100 µl buffer) was added to slides as described above. Slides were incubated overnight in humid chambers at 55°C and were washed four times in 1x SSC at room temperature followed by treatment with 5 µg/ml RNase A (Roche Biomedical Laboratories) in buffer containing 0.5 M NaCl, 10 mM Tris, pH 8.0, and 0.25 mM EDTA, pH 8.0, for 15 min at room temperature. The slides were then washed four times each for 20 min in 0.2x SSC at 60°C, dipped in deionized water, and airdried. All labeled slides were then apposed to X-ray film (Kodak Biomax MR; Eastman Kodak, Rochester, NY) for approximately 14 days.
Film autoradiograms were analyzed using the image analysis program NIH Image (http://www.rsb.info.nih.gov/nih-image 1). Before measurement of sections, the linearity of the videocamera and video capture card to increasing signal intensity was determined using the average gray values of signals of known optical density from a photographic step tablet (Eastman Kodak). The intensity of the light was adjusted such that the values measured from film autoradiograms of brain sections fell within the linear portion of the response of the system. The images of sections from all groups within an experiment that were processed and hybridized in parallel were captured and measured under constant lighting and camera conditions. The striatum was outlined using the image program and the hybridization signal measured in one section per animal at each level of striatum. Measurements were made in the left hemisphere in the rostral (+1.2-1.5 mm anterior to bregma), middle (+0.5 mm anterior to bregma), and caudal (-0.8 mm anterior to bregma) regions of striatum. The number of ppNPY or pSOM mRNA positively labeled particles that exceeded the threshold density in the region of interest was determined using the particle analysis option on NIH Image. The pixel range for particle size was determined before analysis by outlining positively labeled cells from several randomly selected sections and determining the average size of the labeled cells in terms of pixel area. The lower limit for a "labeled cell" on the particle analysis setting was then set to the smallest number of pixels measured for any cell, whereas the upper limit was set at the maximal particle size on the particle analysis option on NIH Image. The threshold density was determined by averaging the density of non-ppNPY- or pSOM-expressing areas taken from several randomly selected sections. The lower threshold was then set to the average background level plus 10 times the standard deviation, whereas the upper level was set at the maximal density. To verify that the ppNPY mRNA-positive particles we were counting were individual cells, subsets of control and multiple METH-treated tissue (n = 8) were labeled for ppNPY mRNA using emulsion autoradiography and counterstained using H&E. The number of clusters of exposed silver grains over an H&E-stained cell correlated significantly with the number of ppNPY mRNA-positive "particles" counted by NIH Image (p = 0.0031; R2 = 0.80). Furthermore, there was no significant difference between the number of silver grain clusters over H&E-stained cells on the emulsion-dipped slides and the number of ppNPY mRNA-positive particles on the film autoradiograms counted by NIH Image (t = 0.8; p = 0.45). Thus, we interpret the number of ppNPY mRNA-positive particles counted by the NIH Image program to be reflective of the number of ppNPY mRNA-positive cells in the dorsal striatum.
The mean density (sum of the gray values of all pixels in the region of interest/number of pixels) of ppNPY and pSOM mRNA labeling in the striatum was also determined for each animal and was expressed as the average gray value for the selected region of interest.
The effects of acute or multiple METH administration on ppNPY or pSOM mRNA expression in the striatum were analyzed using a two-tailed, unpaired t test. The effect of multiple METH treatments on ppNPY mRNA expression in saline-versus SCH22390-pretreated animals or saline-versus eticlopride-pretreated animals was analyzed with a two-way (pretreatment x treatment) analysis of variance for each striatal region. Post hoc analysis of significant effects was accomplished using a Dunnett two-tailed test. The 
level for all analyses was set at 0.05.
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Effect of DA D1 Receptor Blockade on Changes in ppNPY mRNA Expression in the Striatum Induced by Multiple, High Doses of METH. Two-way analysis of variance of the effects of DA D1 receptor blockade on METH-induced ppNPY mRNA expression revealed significant effects of pretreatment and treatment as well as significant pretreatment x treatment interactions throughout the rostrocaudal extent of the striatum (Fig. 4; Table 1). Post hoc analysis revealed that METH treatment significantly increased the number of ppNPY mRNA-positive neurons in rostral (t = -4.4; p = 0.0003), middle (t = -4.0; p = 0.001), and caudal (t = -4.7; p = 0.0001) striatum from saline-pretreated rats but not in the rostral (t = 0.43, p = 0.67), middle (t = 1.6, p = 0.13), or caudal (t = 1.3; p = 0.20) striatum of SCH22390-pretreated animals. The effect of METH was significantly less in SCH22390-pretreated animals than in saline-pretreated animals in the rostral (t = 6.7; p < 0.001), middle (t = 5.4; p < 0.001), and caudal (t = 6.5; p < 0.001) striatum. Neither the multiple METH-dosing regimen nor pretreatment with SCH22390 significantly altered the number of pSOM mRNA-expressing neurons at any level of the striatum examined (Fig. 5).
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Effect of DA D2 Receptor Blockade on Changes in ppNPY mRNA Expression in the Striatum Induced by Multiple, High Doses of METH. Two-way analysis of variance of the effects of DA D2 receptor blockade on METH-induced ppNPY mRNA expression revealed significant effects of pretreatment and treatment as well as significant pretreatment x treatment interactions throughout the rostrocaudal extent of the striatum (Fig. 6; Table 1). Post hoc analysis revealed that METH significantly increased the number of ppNPY mRNA-positive neurons in rostral (t = -5.5; p < 0.0001), middle (t = -6.0; p < 0.0001), and caudal (t = -5.5; p < 0.0001) striatum, relative to saline-pretreated controls. Likewise, eticlopride pretreatment alone significantly increased the number of ppNPY mRNA-positive neurons in the rostral (t = -5.4; p < 0.0001), middle (t = -6.6; p < 0.0001), and caudal (t = -4.6; p < 0.003) regions of striatum. Interestingly, there was no further effect of the multiple METH injections on those animals pretreated with eticlopride in rostral (t = 0.3; p = 0.8), middle (t = -0.12; p = 0.9), and caudal (t = -0.74; t = 0.47) striatum. The number of pSOM mRNA-labeled neurons was not significantly altered by the multiple METH-dosing regimen or pretreatment with eticlopride, at any level of striatum examined (Fig. 7).
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) increases the number of ppNPY mRNA-expressing interneurons in the striatum and that DA D1 receptors play a critical role in multiple-METH-induced changes in ppNPY mRNA expression in the striatum.
It is interesting to note that there was an approximate 20 to 30% increase in the number of neurons expressing ppNPY mRNA in response to multiple doses of METH (Fig. 2). NPY is found only in SOM-positive neurons in the striatum, but approximately 20% of the SOM-positive interneurons do not express NPY under basal conditions, and a small population of SOM-positive neurons expresses DA D1/D5 receptors (Le Moine et al., 1991; Kawaguchi et al., 1995; Rushlow et al., 1995; Figueredo-Cardenas et al., 1996; Rivera et al., 2002). It is possible that this subpopulation of pSOM-positive interneurons in the striatum that basally do not express ppNPY, do so in response to METH treatment, possibly via activation of DA D1/D5 receptors that are present on those interneurons. In line with this hypothesis is the observation that blockade of DA D1 receptors with SCH22390 attenuated the multiple METH-induced increase in the number of ppNPY mRNA-expressing interneurons (Fig. 4).
It is also possible that the increase in ppNPY mRNA in the striatum in response to METH treatment could be due to an interaction between the axon collaterals of striatonigral projection neurons and ppNPY/pSOM-positive interneurons. Striatonigral neurons express SP and DA D1 receptors, whereas pSOM/ppNPY-positive interneurons express the neurokinin-1 receptor for SP (Gerfen, 1992; Kawaguchi, 1997). Activation of DA D1 receptors on striatonigral neurons during METH treatment could enhance SP release from these neurons (Sonsalla et al., 1984), resulting in increased activation of the pSOM/ppNPY-positive neurons. However, if this were the case, there would probably be increased ppNPY mRNA expression in all pSOM-positive neurons, not just a subpopulation of pSOM-positive neurons. Furthermore, there was not a difference in the mean density values for ppNPY mRNA expression per cell in control versus multiple-METH treated animals (data not shown), which supports the notion that the METH-induced changes in ppNPY were not due to general activation of ppNPY/pSOM-positive interneurons.
Alternatively, the increase in the number of ppNPY mRNA-expressing interneurons observed in the present study could be due to multiple METH-induced depletion of DA input to the striatum (Kogan et al., 1976). Previous work has shown that DA depletions increase ppNPY mRNA expression in striatum (Lindefors et al., 1990). However, the present data also show that acute METH treatment, which does not deplete DA input to the striatum (Hotchkiss and Gibb, 1980), increases the number of ppNPY mRNA-expressing interneurons in the striatum to an extent similar to that induced by the neurotoxic regimen. Thus, it is unlikely that the observed changes in ppNPY mRNA expression are the consequence of the toxic effects of multiple METH treatments on nigrostriatal DA neurons, but they more likely reflect activation of DA D1 family receptors on a subset of these interneurons.
It is unclear whether DA D2 receptor antagonism blocks METH-induced changes in ppNPY mRNA expression, because treatment with eticlopride alone produced an increase in the number of ppNPY mRNA-positive neurons similar to that induced by METH, and no further increase in ppNPY mRNA expression was seen in animals also treated with METH. These findings suggest that DA D2 receptor activation is necessary for the METH-induced increases. However, NPY-containing interneurons of the striatum do not express DA D2 or D4 receptors (Le Moine et al., 1991; Rivera et al., 2003). These data may thus also indicate that eticlopride is acting through a similar mechanism as METH to increase the number of ppNPY mRNA-positive interneurons in striatum. Blockade of DA D2 autoreceptors by eticlopride on dopaminergic nigrostriatal nerve terminals increases DA release in the striatum (Herdon et al., 1987; Wong et al., 1995). This eticlopride-induced increase in extracellular DA may activate DA D1 receptors, leading to an increase in ppNPY mRNA-expressing interneurons. Additional studies will be necessary to determine whether SCH23390 can block the eticlopride-induced increase in ppNPY mRNA-expressing neurons.
Previous work suggests that NPY may act as a neuroprotective agent for striatal neurons subject to toxic insults, such as multiple high doses of METH. NPY-positive interneurons in striatum are resistant to excitotoxic injury and METH-induced apoptosis, whereas other striatal neurons are compromised under these conditions (Koh et al., 1986; Beal et al., 1991; Mitchell et al., 1999; Thiriet et al., 2005). Recent work has shown that administration of NPY or NPY receptor agonists prevents METH-induced striatal cell death, whereas NPY knockout mice are more sensitive to METH-induced striatal neuron toxicity (Thiriet et al., 2005). These findings, along with the present data, suggest that increased activation of the NPY system may act as a compensatory response to offset neurotoxic mechanisms activated by METH that contribute to the death of striatal neurons.
Activation of these interneurons may also play a role in METH-induced neurotoxicity to central monoamine systems. NPY is colocalized with nNOS in interneurons of striatum (Kawaguchi et al., 1995), and previous studies indicate that activation of nNOS and subsequent formation of reactive nitrogen species play a role in the neurotoxic effects of METH on striatal monoamine innervation (Itzhak and Ali, 1996; Imam et al., 2001). Furthermore, activation of DA D1 receptors that are expressed only on elements postsynaptic to monoamine terminals in striatum also contributes to METH-induced monoamine toxicity (Sonsalla et al., 1986; O'Dell et al., 1993; Mark et al., 2004), and administration of a DA D1 receptor agonist or amphetamine increases nNOS expression in striatum (Wang and Lau, 2001). The increase in ppNPY mRNA expression observed in the present study may reflect a general DA D1 receptor-mediated activation of a subset of NPY/nNOS-positive neurons that also produce the NO implicated in METH-induced neurotoxicity. Future studies examining whether nNOS and ppNPY are induced in the same interneurons and whether these interneurons also express DA D1 receptors will shed light on this issue.
In summary, the present study is among the first to demonstrate that multiple, high doses of METH increase the number of ppNPY mRNA-expressing neurons in striatum via a DA D1 receptor-mediated mechanism. These findings raise the possibility that a subset of this interneuron population in striatum may be uniquely affected by METH via DA D1 receptor activation. The extent to which activation of this subset of the SOM/NPY/nNOS-containing interneurons plays a role in the neurotoxic potential of METH remains to be determined.
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Footnotes |
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Article, publication date, and citation information can be found at http://jpet.aspetjournals.org.
ABBREVIATIONS: METH, methamphetamine; SP, substance P; nNOS, neuronal nitric-oxide synthase; SOM, somatostatin; NPY, neuropeptide Y; DA, dopamine; pSOM, prosomatostatin; SCH23390, 7-chloro-8-hydoxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benazepine hydrochloride; ppNPY, preproneuropeptide Y; SSC, saline sodium citrate.
Address correspondence to: Dr. Kristen A. Horner, Department of Pharmacology and Toxicology, 30 South 2000 East, Rm 201, University of Utah, Salt Lake City, UT 84112. E-mail: kristen.horner{at}pharm.utah.edu
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References |
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TopAbstractMaterials and MethodsResultsDiscussionReferences |
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Beal MF, Ferrante RJ, Swartz KJ, and Kowall NW (1991) Chronic quinolinic acid lesions in rats closely resemble Huntington's disease. J Neurosci 11: 1649-1659.[Abstract]
Cadet JL, Jayanthi S, and Deng X (2003) Speed kills: cellular and molecular bases of methamphetamine-induced nerve terminal degeneration and neuronal apoptosis. FASEB J 17: 1775-1788.
Deng X, Jayanthi S, Ladenheim B, Krasnova IN, and Cadet JL (2002) Mice with partial deficiency of c-Jun show attenuation of methamphetamine-induced apoptosis. Mol Pharmacol 62: 993-1000.
Deng X, Ladenheim B, Tsao LI, and Cadet JL (1999) Null mutation of c-fos causes exacerbation of methamphetamine-induced neurotoxicity. J Neurosci 19: 10107-101115.
Figueredo-Cardenas G, Morello M, Sancesario G, Bernardi G, and Reiner A (1996) Co-localization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase interneurons in rats. Brain Res 735: 317-324.[CrossRef][Medline]
Fitzpatrick-McElligott S, Card JP, Lewis ME, and Baldino FJ (1988) Neuronal localization of the prosomatostatin mRNA in the rat brain with in situ hybridization histochemistry. J Comp Neurol 273: 558-572.[CrossRef][Medline]
Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15: 133-138.[CrossRef][Medline]
Gerfen CR and Wilson CJ (1996) The basal ganglia, in Handbook of Chemical Neuroanatomy (Swanson LW, Bjorklund A, and Holkfelt T eds) pp 371-465, Elsevier Science, London.
Herdon H, Strupish H, and Nahorski SR (1987) Endogenous DA release from rat striatal slices and its regulation by D-2 autoreceptors: effects of uptake inhibitors and synthesis inhibition. Eur J Pharmacol 138: 69-76.[CrossRef][Medline]
Hotchkiss AJ and Gibb JW (1980) Long-term effects of multiple doses of metham-phetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J Pharmacol Exp Ther 214: 257-262.
Imam SZ, Newport GD, Itzhak Y, Cadet JL, Islam F, Slikker W, and Ali SF (2001) Peroxynitrite plays a role in methamphetamine-induced dopaminergic neurotoxicity: evidence from mice lacking neuronal nitric oxide synthase gene or overexpressing copper-zinc superoxide dismutase. J Neurochem 76: 745-749.[CrossRef][Medline]
Itzhak Y and Ali SF (1996) The neuronal nitric oxide synthase inhibitor, 7-nitroindazole, protects against methamphetamine-induced neurotoxicity in vivo. J Neurochem 67: 1770-1773.[Medline]
Kawaguchi Y (1997) Neostriatal cell subtypes and their functional roles. Neurosci Res 27: 1-8.[CrossRef][Medline]
Kawaguchi Y, Wilson CJ, Augood SJ, and Emson PC (1995) Striatal interneurones: Chemical, physiological and morphological characterization. Trends Neurosci 18: 527-535.[CrossRef][Medline]
Kogan FJ, Nichols WK, and Gibb JW (1976) Influence of methamphetamine on nigral and striatal tyrosine hydroxylase activity and on striatal dopamine levels. Eur J Pharmacol 36: 363-371.[CrossRef][Medline]
Koh JY, Peters S, and Choi DW (1986) Neurons containing NADPH-diaphorase are selectively resistant to quinolinate toxicity. Science (Wash DC) 234: 73-76.
Kubota Y, Inagaki S, Kito S, Shimada S, Okayama T, Hatanaka H, Pelletier G, Takagi H, and Tobyama M (1988) Neuropeptide Y-immunoreactive neurons receive synaptic inputs from dopaminergic axon terminals in the rat neostriatum. Brain Res 458: 389-393.[CrossRef][Medline]
Larhammar D, Ericson A, and Persson H (1987) Structure and expression of the rat neuropeptide Y gene. Proc Natl Acad Sci USA 84: 2068-2072.
Le Moine C, Normand E, and Bloch B (1991) Phenotypical characterization of the rat striatal neurons expressing the D1 dopamine receptor gene. Proc Natl Acad Sci USA 88: 4205-4209.
Lindefors N, Brene S, Herrera-Marschitz A, and Persson H (1990) Neuropeptide gene expression in the brain is differentially regulated by midbrain dopamine neurons. Exp Brain Res 419: 403-407.
Mark KA, Soghomonian JJ, and Yamamoto BK (2004) High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J Neurosci 24: 11449-11456.
Mitchell IJ, Cooper AJ, and Griffiths MR (1999) The selective vulnerability of striatopallidal neurons. Prog Neurobiol 59: 691-719.[CrossRef][Medline]
O'Dell S, Weihmeuller FB, and Marshall JF (1993) Methamphetamine-induced dopamine overflow and injury to striatal dopamine terminals: attenuation by dopamine D1 or D2 antagonists. J Neurochem 60: 1792-1799.[Medline]
Rivera A, Alberti I, Martin AB, Narvaez JA, de la Calle A, and Moratalla R (2002) Molecular phenotype of rat striatal neurons expressing the dopamine D5 receptor subtype. Eur J Neurosci 16: 2049-2058.[CrossRef][Medline]
Rivera A, Trias S, Penafiel A, Angetl Narvaez J, Diaz-Cabiale Z, Moratalla R, and de la Calle A (2003) Expression of D4 dopamine receptors in striatonigral and stria-topallidal neurons in the rat striatum. Brain Res 989: 35-41.[CrossRef][Medline]
Rushlow W, Flumerfelt BA, and Naus CCG (1995) Co-localization of somatostatin, neuropeptide Y and NADPH-diaphorase in the caudate putamen of the rat. J Comp Neurol 351: 499-508.[CrossRef][Medline]
Sonsalla PK, Gibb JW, and Hanson GR (1984) Opposite responses in the striatonigral substance P system to D1 and D2 receptor activation. Eur J Pharmacol 105: 185-187.[CrossRef][Medline]
Sonsalla PK, Gibb JW, and Hanson GR (1986) Roles of D1 and D2 dopamine receptor subtypes in mediating the methamphetamine-induced changes in monoamine systems. J Pharmacol Exp Ther 238: 932-937.
Thiriet N, Deng X, Solinas M, Ladenheim B, Curtis W, Goldberg SR, Palmiter RD, and Cadet JL (2005) Neuropeptide Y protects against methamphetamine-induced neuronal apoptosis in the mouse striatum. J Neurosci 25: 5273-5279.
Vincent SR, Johansson O, Hokfelt T, Skirboll L, Elde RP, Terenius L, Kimmel J, and Goldstein M (1983) NADPH-diaphorase: a selective histochemical marker for striatal neurons containing both somatostatin and avian pancreatic polypeptide (APP)-like immunoreactivities. J Comp Neurol 217: 252-263.[CrossRef][Medline]
Volkow ND, Chang L, Wang GJ, Fowler JS, Franscechi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Wong C, et al. (2001) Higher cortical and lower subcortical metabolism in detoxified methamphetamine abusers. Am J Psychiatry 158: 383-389.
Wang JQ and Lau Y-S (2001) Dose-related alteration in nitric oxide synthase mRNA expression induced by amphetamine and the full D1 dopamine receptor agonist SKF-82958 in mouse striatum. Neurosci Lett 311: 5-8.[CrossRef][Medline]
Westwood SC and Hanson GR (1999) Effects of stimulants of abuse on extrapyrimidal and limbic neuropeptide Y systems. J Pharmacol Exp Ther 288: 1160-1166.
Wilson JM, Kalasinsky KS, Levey AI, Bergeron C, Reiber G, Anthony RM, Schmunk GA, Shannak K, Haycock JW, and Kish SJ (1996) Striatal dopamine nerve terminal markers in human, chronic methamphetamine users. Nat Med 2: 699-703.[CrossRef][Medline]
Wong PT, Feng H, and Teo WL (1995) The interaction of the dopaminergic and serotonergic systems in rat striatum: effects of selective antagonists and inhibitors. Neurosci Res 23: 115-119.[Medline]
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