Differential Effect of the Dopamine Agonist ( )-7-Hydroxy-2-(N,N-di-n-propylamino) Tetralin (7-OH-DPAT) on Motor Activity between Adult Wistar and Sprague-Dawley Rats after a Neonatal Ventral Hippocampus Lesion
The neonatal ventral hippocampal lesion (nVHL) has been widely used as an animal model for schizophrenia. Rats with an nVHL show several delayed behavioral alterations that mimic some symptoms of schizophrenia. Sprague-Dawley (SD) rats with an nVHL have a decrease in D3 receptors in limbic areas, but the expression of D3 receptors in Wistar (W) rats with an nVHL is unknown. The 7-Hydroxy-2-(N,N-di-n-propylamino) tetralin (7-OH-DPAT) has been reported as a D3-preferring agonist. Thus, we investigated the effect of ( )-7-OH-DPAT (0.25?mg/kg) on the motor activity in male adult W and SD rats after an nVHL. The 7-OH-DPAT caused a decrease in locomotion of W rats with an nVHL, but it did not change the locomotion of SD rats with this lesion. Our results suggest that the differential effect of 7-OH-DPAT between W and SD rats with an nVHL could be caused by a different expression of the D3 receptors. These results may have implications for modeling interactions of genetic and environmental factors involved in schizophrenia. 1. Introduction Dopamine (DA) receptors are classified into two broad families, namely, the D1-like (D1 and D5) and D2-like (D2, D3, and D4) receptors [1]. The D3 receptor was first cloned and characterized by Sokoloff et al. in 1990 [2]. It is negatively coupled to adenylate cyclase. In rats, the D3 receptor is mostly distributed in projection areas of the mesocorticolimbic dopaminergic system, for example, the nucleus accumbens, olfactory tubercle, islands of Calleja, and prefrontal cortex [3–6]. Although the role of the D3 receptor in the brain function has not been completely established, it has been related to behavioral aspects such as locomotion, emotion, and cognition [6–11]. The D3 receptor has also been implicated in disorders, such as schizophrenia and drug abuse, because its pharmacology and pattern of location in the brain is consistent with defective neural circuits seen in such disorders [12, 13]. For example, postmortem studies suggest a D3 receptor dysfunctionality in some cortical regions of brains obtained from schizophrenic patients [14, 15]. The locomotor responses to novelty and psychostimulants seem to be regulated by D3 receptors [6, 10, 16, 17]. 7-Hydroxy-2-(N,N-di-n-propylamino) tetralin (7-OH-DPAT) has been described as a D3-preferring agonist [4, 18]. In rats, administration of low doses of 7-OH-DPAT decreases locomotion, with such reduction in locomotion attributed to a D3 autoreceptor stimulation [7], but some findings suggest that the inhibitory action of the D3 receptors on locomotion can also occur via
References
[1]
C. Missale, S. R. Nash, S. W. Robinson, M. Jaber, and M. G. Caron, “Dopamine receptors: from structure to function,” Physiological Reviews, vol. 78, no. 1, pp. 189–225, 1998.
[2]
P. Sokoloff, B. Giros, M. P. Martres, M. L. Bouthenet, and J. C. Schwartz, “Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics,” Nature, vol. 347, no. 6289, pp. 146–151, 1990.
[3]
G. Flores, D. Barbeau, R. Quirion, and L. K. Srivastava, “Decreased binding of dopamine D3 receptors in limbic subregions after neonatal bilateral lesion of rat hippocampus,” Journal of Neuroscience, vol. 16, no. 6, pp. 2020–2026, 1996.
[4]
D. Levesque, J. Diaz, C. Pilon et al., “Identification, characterization, and localization of the dopamine 3D receptor in rat brain using 7-[3H]hydroxy-N,N-di-n-propyl-2-aminotetralin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 17, pp. 8155–8159, 1992.
[5]
J. Diaz, C. Pilon, B. Le Foll et al., “Dopamine D3 receptors expressed by all mesencephalic dopamine neurons,” Journal of Neuroscience, vol. 20, no. 23, pp. 8677–8684, 2000.
[6]
J. Flores-Tochihuitl, G. Vargas, J. C. Morales-Medina et al., “Enhanced apomorphine sensitivity and increased binding of dopamine D2 receptors in nucleus accumbens in prepubertal rats after neonatal blockade of the dopamine D3 receptors by (+)-S14297,” Synapse, vol. 62, no. 1, pp. 40–49, 2008.
[7]
S. A. Daly and J. L. Waddington, “Behavioural effects of the putative D-3 dopamine receptor agonist 7-OH-DPAT in relation to other “D-2-like” agonists,” Neuropharmacology, vol. 32, no. 5, pp. 509–510, 1993.
[8]
K. Svensson, A. Carlsson, and N. Waters, “Locomotor inhibition by the D3 ligand R-(+)-7-OH-DPAT is independent of changes in dopamine release,” Journal of Neural Transmission-General Section, vol. 95, no. 1, pp. 71–74, 1994.
[9]
L. Chagas-Martinich, R. J. Carey, and M. P. Carrera, “7-OH-DPAT effects on latent inhibition: low dose facilitation but high dose blockade: implications for dopamine receptor involvement in attentional processes,” Pharmacology Biochemistry and Behavior, vol. 86, no. 3, pp. 441–448, 2007.
[10]
L. M. Pritchard, A. D. Logue, B. C. Taylor et al., “Relative expression of D3 dopamine receptor and alternative splice variant D3nf mRNA in high and low responders to novelty,” Brain Research Bulletin, vol. 70, no. 4–6, pp. 296–303, 2006.
[11]
C. Wilson and M. Pulido, “Effects of the dopamine antagonist PD 152255 on Juvenile rats' responses to dorsal stimulation, the transport response, and related behaviors,” Behavioral Neuroscience, vol. 116, no. 6, pp. 1098–1102, 2002.
[12]
J. C. Schwartz, J. Diaz, C. Pilon, and P. Sokoloff, “Possible implications of the dopamine D(3) receptor in schizophrenia and in antipsychotic drug actions,” Brain Research Reviews, vol. 31, no. 2-3, pp. 277–287, 2000.
[13]
M. Pilla, S. Perachon, F. Sautel et al., “Selective inhibition of cocaine-seeking behaviour by a partial dopamine D3 receptor agonist,” Nature, vol. 400, no. 6742, pp. 371–375, 1999.
[14]
C. Schmauss, “Enhanced cleavage of an atypical intron of dopamine D3-receptor pre- mRNA in chronic schizophrenia,” Journal of Neuroscience, vol. 16, no. 24, pp. 7902–7909, 1996.
[15]
C. Schmauss, V. Haroutunian, K. L. Davis, and M. Davidson, “Selective loss of dopamine D3-type receptor mRNA expression in parietal and motor cortices of patients with chronic schizophrenia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 19, pp. 8942–8946, 1993.
[16]
R. K. McNamara, A. Logue, K. Stanford, M. Xu, J. Zhang, and N. M. Richtand, “Dose-response analysis of locomotor activity and stereotypy in dopamine D3 receptor mutant mice following acute amphetamine,” Synapse, vol. 60, no. 5, pp. 399–405, 2006.
[17]
L. M. Pritchard, A. D. Logue, S. Hayes et al., “7-OH-DPAT and PD 128907 selectively activate the D3 dopamine receptor in a novel environment,” Neuropsychopharmacology, vol. 28, no. 1, pp. 100–107, 2003.
[18]
M. Hillefors-Berglund and G. Von Euler, “Pharmacology of dopamine D3 receptors in the islands of Calleja of the rat using quantitative receptor autoradiography,” European Journal of Pharmacology, vol. 261, no. 1-2, pp. 179–183, 1994.
[19]
N. Waters, K. Svensson, S. R. Haadsma-Svensson, M. W. Smith, and A. Carlsson, “The dopamine D3-receptor: a postsynaptic receptor inhibitory on rat locomotor activity,” Journal of Neural Transmission-General Section, vol. 94, no. 1, pp. 11–19, 1993.
[20]
S. H. Fatemi and T. D. Folsom, “The neurodevelopmental hypothesis of schizophrenia, revisited,” Schizophrenia Bulletin, vol. 35, no. 3, pp. 528–548, 2009.
[21]
K. Y. Tseng, R. A. Chambers, and B. K. Lipska, “The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia,” Behavioural Brain Research, vol. 204, no. 2, pp. 295–305, 2009.
[22]
B. K. Lipska, G. E. Jaskiw, and D. R. Weinberger, “Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia,” Neuropsychopharmacology, vol. 9, no. 1, pp. 67–75, 1993.
[23]
F. Sams-Dodd, B. K. Lipska, and D. R. Weinberger, “Neonatal lesions in the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood,” Psychopharmacology, vol. 132, no. 3, pp. 303–310, 1997.
[24]
A. Becker, G. Grecksch, H. G. Bernstein, V. H?llt, and B. Bogerts, “Social behaviour in rats lesioned with ibotenic acid in the hippocampus: quantitative and qualitative analysis,” Psychopharmacology, vol. 144, no. 4, pp. 333–338, 1999.
[25]
J. P. Marquis, S. Goulet, and F. Y. Doré, “Neonatal lesions of the ventral hippocampus in rats lead to prefrontal cognitive deficits at two maturational stages,” Neuroscience, vol. 140, no. 3, pp. 759–767, 2006.
[26]
R. A. Chambers, J. Moore, J. P. McEvoy, and E. D. Levin, “Cognitive effects of neonatal hippocampal lesions in a rat model of schizophrenia,” Neuropsychopharmacology, vol. 15, no. 6, pp. 587–594, 1996.
[27]
B. K. Lipska, J. M. Aultman, A. Verma, D. R. Weinberger, and B. Moghaddam, “Neonatal damage of the ventral hippocampus impairs working memory in the rat,” Neuropsychopharmacology, vol. 27, no. 1, pp. 47–54, 2002.
[28]
G. K. Wood, R. Quirion, and L. K. Srivastava, “Early environment contributes to developmental disruption of MPFC after neonatal ventral hippocampal lesions in rats,” Synapse, vol. 50, no. 3, pp. 223–232, 2003.
[29]
H. A. Al-Amin, D. R. Weinberger, and B. K. Lipska, “Exaggerated MK-801-induced motor hyperactivity in rats with the neonatal lesion of the ventral hippocampus,” Behavioural Pharmacology, vol. 11, no. 3-4, pp. 269–278, 2000.
[30]
T. Hori, S. Subramaniam, L. K. Srivastava, and R. Quirion, “Behavioral and neurochemical alterations following repeated phencyclidine administration in rats with neonatal ventral hippocampal lesions,” Neuropharmacology, vol. 39, no. 12, pp. 2478–2491, 2000.
[31]
V. Blas-Valdivia, E. Cano-Europa, A. Hernández-García, and R. Ortiz-Butrón, “Neonatal bilateral lidocaine administration into the ventral hippocampus caused postpubertal behavioral changes: an animal model of neurodevelopmental psychopathological disorders,” Neuropsychiatric Disease and Treatment, vol. 5, no. 1, pp. 15–22, 2009.
[32]
K. S. Alexander, J. M. Brooks, M. Sarter, and J. P. Bruno, “Disruption of mesolimbic regulation of prefrontal cholinergic transmission in an animal model of schizophrenia and normalization by chronic clozapine treatment,” Neuropsychopharmacology, vol. 34, no. 13, pp. 2710–2720, 2009.
[33]
S. Bekris, K. Antoniou, S. Daskas, and Z. Papadopoulou-Daifoti, “Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains,” Behavioural Brain Research, vol. 161, no. 1, pp. 45–59, 2005.
[34]
E. L. Abel, “Response to alarm substance in different rat strains,” Physiology and Behavior, vol. 51, no. 2, pp. 345–347, 1992.
[35]
S. Zamudio, T. Fregoso, A. Miranda, F. De La Cruz, and G. Flores, “Strain differences of dopamine receptor levels and dopamine related behaviors in rats,” Brain Research Bulletin, vol. 65, no. 4, pp. 339–347, 2005.
[36]
G. G. Kinney, L. O. Wilkinson, K. L. Saywell, and M. D. Tricklebank, “Rat strain differences in the ability to disrupt sensorimotor gating are limited to the dopaminergic system, specific to prepulse inhibition, and unrelated to changes in startle amplitude or nucleus accumbens dopamine receptor sensitivity,” Journal of Neuroscience, vol. 19, no. 13, pp. 5644–5653, 1999.
[37]
P. K. Pilz, R. Linke, D. M. Yilmazer-Hanke, and H. Schwegler, “Comparison of two sensitization paradigms of the acoustic startle response in Wistar and Sprague-Dawley rats,” Behavior Genetics, vol. 29, no. 1, pp. 59–63, 1999.
[38]
I. C. Weiss, L. Di Iorio, J. Feldon, and A. M. Domeney, “Strain differences in the isolation-induced effects on prepulse inhibition of the acoustic startle response and on locomotor activity,” Behavioral Neuroscience, vol. 114, no. 2, pp. 364–373, 2000.
[39]
A. Rex, J. P. Voigt, C. Gustedt, S. Beckett, and H. Fink, “Anxiolytic-like profile in Wistar, but not Sprague-Dawley rats in the social interaction test,” Psychopharmacology, vol. 177, no. 1-2, pp. 23–34, 2004.
[40]
K. Y. Tseng, B. L. Lewis, T. Hashimoto et al., “A neonatal ventral hippocampal lesion causes functional deficits in adult prefrontal cortical interneurons,” Journal of Neuroscience, vol. 28, no. 48, pp. 12691–12699, 2008.
[41]
H. A. Al Amin, S. F. Atweh, S. J. Jabbur, and N. E. Saadé, “Effects of ventral hippocampal lesion on thermal and mechanical nociception in neonates and adult rats,” European Journal of Neuroscience, vol. 20, no. 11, pp. 3027–3034, 2004.
[42]
A. Sierra, I. Camacho-Abrego, J. V. Negrete-Díaz, L. Rodríguez-Sosa, C. Escamilla, and G. Flores, “Economical body platform for neonatal rats stereotaxic surgery,” Revista de Neurologia, vol. 48, no. 3, pp. 141–146, 2009.
[43]
B. K. Lipska and D. R. Weinberger, “Genetic variation in vulnerability to the behavioral effects of neonatal hippocampal damage in rats,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 19, pp. 8906–8910, 1995.
[44]
G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, New York, NY, USA, 1986.
[45]
M. López-Martínez, H. Salgado-Zamora, E. R. San-Juan, et al., “Anti-anxiety and sedative profile evaluation of imidazo[1,2-a]pyridine derivatives,” Drug Development Research, vol. 71, no. 6, pp. 371–381, 2010.
[46]
K. Frantz, D. Babcock, and C. Van Hartesveldt, “The locomotor effects of a putative dopamine D3 receptor agonist in developing rats,” European Journal of Pharmacology, vol. 302, no. 1–3, pp. 1–6, 1996.
[47]
T. V. Khroyan, D. A. Baker, R. A. Fuchs, N. Manders, and J. L. Neisewander, “Differential effects of 7-OH-DPAT on amphetamine-induced stereotypy and conditioned place preference,” Psychopharmacology, vol. 139, no. 4, pp. 332–341, 1998.
[48]
P. De Boer, P. Enrico, J. Wright et al., “Characterization of the effect of dopamine D3 receptor stimulation on locomotion and striatal dopamine levels,” Brain Research, vol. 758, no. 1-2, pp. 83–91, 1997.
[49]
T. Kling-Petersen, E. Ljung, and K. Svensson, “Effects on locomotor activity after local application of D3 preferring compounds in discrete areas of the rat brain,” Journal of Neural Transmission-General Section, vol. 102, no. 3, pp. 209–220, 1995.
[50]
A. M. Ouagazzal and I. Creese, “Intra-accumbens infusion of D(3) receptor agonists reduces spontaneous and dopamine-induced locomotion,” Pharmacology Biochemistry and Behavior, vol. 67, no. 3, pp. 637–645, 2000.
[51]
L. Zhang, D. Lou, H. Jiao et al., “Cocaine-induced intracellular signaling and gene expression are oppositely regulated by the dopamine D1 and D3 receptors,” Journal of Neuroscience, vol. 24, no. 13, pp. 3344–3354, 2004.
[52]
M. Xu, T. E. Koeltzow, G. T. Santiago et al., “Dopamine D3 receptor mutant mice exhibit increased behavioral sensitivity to concurrent stimulation of D1 and D2 receptors,” Neuron, vol. 19, no. 4, pp. 837–848, 1997.
[53]
S. Ahlenius and P. Salmi, “Behavioral and biochemical effects of the dopamine D3 receptor-selective ligand, 7-OH-DPAT, in the normal and the reserpine-treated rat,” European Journal of Pharmacology, vol. 260, no. 2-3, pp. 177–181, 1994.
[54]
R. Depoortere, G. Perrault, and D. J. Sanger, “Behavioural effects in the rat of the putative dopamine D3 receptor agonist 7-OH-DPAT: comparison with quinpirole and apomorphine,” Psychopharmacology, vol. 124, no. 3, pp. 231–240, 1996.
[55]
B. Levant, G. N. Bancroft, and C. M. Selkirk, “In vivo occupancy of D2 dopamine receptors by 7-OH-DPAT,” Synapse, vol. 24, no. 1, pp. 60–64, 1996.
[56]
D. B. Gilbert and S. J. Cooper, “7-OH-DPAT injected into the accumbens reduces locomotion and sucrose ingestion: D3 autoreceptor-mediated effects?” Pharmacology Biochemistry and Behavior, vol. 52, no. 2, pp. 275–280, 1995.
[57]
R. R. Gainetdinov, T. D. Sotnikova, T. V. Grekhova, and K. S. Rayevsky, “In vivo evidence for preferential role of dopamine D3 receptor in the presynaptic regulation of dopamine release but not synthesis,” European Journal of Pharmacology, vol. 308, no. 3, pp. 261–269, 1996.
[58]
T. E. Koeltzow, M. Xu, D. C. Cooper et al., “Alterations in dopamine release but not dopamine autoreceptor function in dopamine D3 receptor mutant mice,” Journal of Neuroscience, vol. 18, no. 6, pp. 2231–2238, 1998.
[59]
J. D. Joseph, Y. M. Wang, P. R. Miles, et al., “Dopamine autoreceptor regulation of release and uptake in mouse brain slices in the absence of D(3) receptors,” Neuroscience, vol. 112, no. 1, pp. 39–49, 2002.
[60]
Y. Goto and P. O'Donnell, “Delayed mesolimbic system alteration in a developmental animal model of schizophrenia,” Journal of Neuroscience, vol. 22, no. 20, pp. 9070–9077, 2002.
[61]
K. Liu, C. Bergson, R. Levenson, and C. Schmauss, “On the origin of mRNA encoding the truncated dopamine D3-type receptor D3nf and detection of D3nf-like immunoreactivity in human brain,” Journal of Biological Chemistry, vol. 269, no. 46, pp. 29220–29226, 1994.
[62]
E. W. Daenen, G. Wolterink, J. A. Van Der Heyden, C. G. Kruse, and J. M. Van Ree, “Neonatal lesions in the amygdala or ventral hippocampus disrupt prepulse inhibition of the acoustic startle response; implications for an animal model of neurodevelopmental disorders like schizophrenia,” Neuropsychopharmacology, vol. 13, no. 3, pp. 187–197, 2003.
[63]
G. Flores, G. K. Wood, D. Barbeau, R. Quirion, and L. K. Srivastava, “Lewis and Fischer rats: a comparison of dopamine transporter and receptors levels,” Brain Research, vol. 814, no. 1-2, pp. 34–40, 1998.