Abstract
Differences in pharmacology, anatomical connections, and receptor densities between the “core” and “shell” of the nucleus accumbens suggest that behavioral activity normally modulated by the accumbens, such as reward and motor functions, may be differentially regulated across the mediolateral axis. This study investigated the effects of opiate receptor-specific agonists on reward and motor functions in either the accumbens core or shell, using the intracranial self-stimulation (ICSS) rate-frequency curve-shift method. Microinjections of the mu opiate receptor-specific agonist, DAMGO (vehicle, 0.03 nmol, and 0.3 nmol), or the delta opiate receptor-specific agonist DPDPE (vehicle, 0.3 nmol, 3.0 nmol), were administered bilaterally in a random dose order with a minimum of 3 days between injections. Rats were tested over three consecutive 20-min rate-frequency curves immediately following a microinjection to investigate the time course of drug effects. Both opiate agonists decreased the ICSS frequency necessary to maintain half-maximal response rates when injected into the medial and ventral shell region of the accumbens. However, DAMGO microinjections into the lateral accumbens core or the control site of the caudate increased the frequency necessary to elicit half-maximal response rates, while DPDPE microinjections into these regions had no effect. Evaluation of motor effects show that administration of DAMGO resulted in a suppression of activity in all locations. In contrast, DPDPE microinjections resulted in little or no effect on lever pressing activity at any location.
Similar content being viewed by others
References
Berendse HW, Galis-de-Graff Y, Groenewegen HJ (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316:314–347
Campbell KA, Evans G, Gallistel CR (1985) A microcomputer-based method for physiologically interpretable measurement of the rewarding efficacy of brain stimulation. Physiol Behav 35:395–403
Cunningham ST, Kelley AE (1992a) Evidence for opiate-dopamine cross-sensitization in nucleus accumbens: studies of conditioned reward. Brain Res Bull 29:675–680
Cunningham TS, Kelley AE (1992b) Opiate infusion into nucleus accumbens: contrasting effects on motor activity and responding for conditioned reward. Brain Res 588:104–114
Deutch AY, Cameron DS (1992) Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell. Neuroscience 46:49–56
Dilts RP, Kalivas PW (1990) Autoradiographic localization of delta opioid receptors within the mesocorticolimbic dopamine system using radioiodinated [2-d-penicillamine, 5-d-penicillamine] enkephalin (125I-DPDPE). Synapse 6:121–132
Dworkin SI, Guerin GF, Co C, Goeders NE, Smith JE (1988) Lack of an effect of 6-hydroxydopamine lesions of the nucleus accumbens on intravenous morphine self-administration. Pharmacol Biochem Behav 30:1051–1057
Edmonds DE, Gallistel CR (1974) Parametric analysis of brain stimulation reward in the rat: effect of performance variables on the reward summation function. J Comp Physiol Psychol 87:876–883
Essman WD, McGonigle P, Lucki I (1993) Anatomical differentiation within the nucleus accumbens of the locomotor stimulatory actions of selective dopamine agonists andd-amphetamine. Psychopharmacology 112:233–241
Groenewegen HJ, Groenewegen HJ, Vermeulen-Van der Zee E, te Kortschot A, Witter MP (1987) Organization of the projections from the subiculum to the ventral striatum of the rat. A study using anterograde transport ofphaseolus vulgaris-leucoagglutinin. Neuroscience 23:103–120
Haber SN, Lynd-Balta E, Mitchell SJ (1993) The organization of the decending ventral pallidal projection in the monkey. J Comp Neurol 329:111–128
Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89–125
Herkenham M, Moon Edley S, Stuart J (1984) Cell clusters in the nucleus accumbens of the rat, the mosaic relationship of opiate receptors, acetylcholinesterase and subcortical afferent terminations. Neuroscience 11:561–593
Johnson PI, Stellar JR (1994)N-Methyl-d-aspartic acid-induced lesions of the nucleus accumbens and/or ventral pallidum fail to attenuate lateral hypothalamic self-stimulation reward. Brain Res 646:73–84
Johnson PI, Stellar JR, Parente MA (1994) Excitotoxic lesions of the nucleus accumbens or the ventral pallidum suggest a mediolateral regulation of reward function in food deprived rats. Soc Neurosci Abstr 20:156.7, p 366
Jongen-Rêlo AL, Groenewegen HJ, Voorn P (1993) Evidence for a multi-compartmental histochemical organization of the nucleus accumbens in the rat. J Comp Neurol 337:267–276
Jongen-Rêlo AL, Voorn P, Groenewegen HJ (1994) Immunohistochemical characterization of the shell and core territories of the nucleus accumbens in the rat. Eur J Neurosci (in press)
Maldonado-Irizarry CS, Kelley AE (1993) Evidence for behavioral dissociation between “core” and “shell” subregions of the nucleus accumbens following microinjections of DNQX, a non-NMDA antagonist. Soc Neurosci Abstr 19:329.17, p 812
Maldonado-Irizarry CS, Kelley AE (1994) Differential behavioral effects following microinjection of an NMDA antagonist into nucleus accumbens subregions. Psychopharmacology 116:65–72
Martin GE, Blank B, Groenewegen HJ (1991) The striatal mosaic in primates: patterns of neuropeptide immunoreactivity differentiate the ventral striatum from the dorsal striatum. Neuroscience 43:397–417
Maxwell SE, Delaney HD (1990) One-way within-subjects design: univariate approach. In: Designing experiments and analysing data. Wadsworth, CA, pp 456–494
Olds ME (1982) Reinforcing effects of morphine in the nucleus accumbens Brain Res 237:429–440
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, Orlando, Fla.
Smith JE, Guerin GF, Co C, Barr TS, Lane JD (1985) Effects of 6-OHDA lesions of the central medial nucleus accumbens on rat intravenous morphine self-administration. Pharmacol Biochem Behav 23:843–849
Stellar JR, Rice M (1989) Pharmacological basis of intracranial self-stimulation reward. In: Lieberman JM, Cooper SJ (eds) Neuropharmacological basis of reward. Oxford Press, New York, pp 14–65
Stellar JR, Waraczynski M, Wong K (1988) The reward summation function in hypothalamic self-stimulation. In: Commons ML, Church RM, Stellar JR, Wagner AR (eds) Quantitative analysis of behavior. Lawrence Erlbaum, New Jersey, pp 31–57
Van der Kooy D, Mucha RF, O'Shaughnessy M, Bucenieks, P (1982) Reinforcing effects of brain microinjections of morphine revealed by conditioned place preference. Brain Res 243:107–117
Voorn P, Gerfen CR, Groenewegen HJ (1989) Compartmental organization of the ventral striatum of the rat: immunohistochemical distribution of enkephalin, substance P, dopamine, calcium-binding protein. J Comp Neurol 289:189–201
West TEG, Wise RA (1989) Nucleus accumbens injections of mu and delta but not kappa opioids facilitate hypothalamic brain stimulation reward. Soc Neurosci Abstr 15:20.8, p 34
Witter MP, Ostendorf RH, Groenewegen HJ (1990) Heterogeneity in the dorsal subiculum of the rat. Distinct neuronal zones project to different cortical and subcortical targets. Eur J Neurosci 2:718–725
Záborszky L, Alheid GF, Beinfeld MC, Eiden LE, Heimer L, Palkovits M (1985) Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14:427–453
Zahm DS (1989) The ventral striatopallidal parts of the basal ganglia in the rat — II Compartmentation of ventral pallidal efferents Neuroscience 30:33–50
Zahm DS, Brog JS (1992) Commentary on the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience 50:751–767
Zahm DS, Heimer L (1988) Ventral striatopallidal parts of the basal ganglia in the rat: I Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreactivity. J Comp Neurol 272:516–535
Zahm DS, Heimer L (1990) Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol 302:437–446
Zahm DS, Heimer L (1993) Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220–232
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Johnson, P.I., Goodman, J.B., Condon, R. et al. Reward shifts and motor responses following microinjections of opiate-specific agonists into either the core or shell of the nucleus accumbens. Psychopharmacology 120, 195–202 (1995). https://doi.org/10.1007/BF02246193
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02246193