Abstract
Neuropeptide substance P (SP) has reinforcing and memory facilitating effects after its peripheral or central application. Rats self-inject SP into the ventromedial caudate-putamen and SP microinjections into the basal forebrain induce place preference with a simultaneous increase of dopamine level. In the amygdaloid body SP positive neurones and terminals have been identified. The aim of the present study was to examine the possible reinforcing effects of SP in the basolateral amygdala (ABL). CFY male rats were conditioned in two-compartment passive avoidance paradigm and place preference was examined in two-compartment-box and in circular open field. Animals were microinjected bilaterally with 10 ng SP, 100 ng SP or vehicle solution (0.4 μl/side) into the ABL. Results showed that post-shock infusion of 10 ng SP significantly enhanced passive avoidance learning while 100 ng SP was ineffective. In two-compartment-box and in circular open field place preference did not develop after SP treatments, however. Our data are the first to demonstrate that SP in the ABL is involved in learning and memory processes related to aversive situations. Results that SP microinjections were not followed by rewarding-reinforcing consequences in place preference paradigms indicate that the local SP network in the ABL is not involved in neuronal circuitry responsible for addictive behaviour.
Article PDF
Similar content being viewed by others
References
Ben-Ari, Y., Zigmond, R. E., Moore, K. E. (1978) Regional distribution of thyrosine hydroxylase, norepinephrine and dopamine within the amygdaloid complex of the rat. Brain Res. 87, 96–101.
Boix, F., Sándor, P., Nogueira, P. J. C., Huston, P. J., Schwarting, R. K. W. (1995) Relationship between dopamine release in nucleus accumbens and place preference induced by substance P injected into the nucleus basalis magnocellularis region. Neuroscience 64, 1045–1055.
Dworkin, S. I., Goeders, N. E., Smith, J. M. (1985) The reinforcing and rate effects of intracranial dopamine administration. Nat. Inst. Drug Abuse Res., Monograph Series 67, 242–248.
Gerhardt, P., Hasenöhrl, R. U., Huston, J. P. (1992) Enhanced learning produced by injection of neu-rokinin substance P into the region of the nucleus basalis magnocellularis: mediation by the N-ter-minal sequence. Exp. Neurol., 118, 302–308.
Grossmann, S. P., Grossmann, L., Walsh, L. (1975) Functional organization of the rat amygdala with respect to avoidance behavior. J. Comp. Physiol. Psychol. 88, 829–850.
Hall, M., Stewart, J. (1983) Substance P and analgesia. Peptides 4, 31–35.
Hoebel, B. G., Monaco, A. P., Hernandez, L., Stanley, B. G., Aulisi, E. F., Lénárd, L. (1983) Self-injection of amphetamine directly into the brain. Psychopharmacol. 81, 158–164.
Holzhauer-Oitzl, M. S., Boucke, K., Huston, J. P. (1987) Reinforcing properties of substance P in the lateral hypothalamus revealed by conditioned place preference. Pharmac. Biochem. Behav. 28, 511–515.
Huston, J. P., Hasenöhrl, R. U. (1995) The role of neuropeptides in learning: focus on the neurokinin substance P. Behav. Brain Res. 66, 117–127.
Huston, J. P., Oitzl, M. S. (1989) The relationship between reinforcement and memory: Parallels in the rewarding and mnemonic effects of the neuropeptide substance P. Neurosci. Biobehav. Rev. 13, 171–180.
Huston, J. P., Staubli, U. (1979) Post-trial injection of substance P into the lateral hypothalamus and amygdala, respectively, facilitates and impairs learning. Behav. Neural Biol. 27, 244–248.
Iversen, L. (1982) Substance P. Br. Med. Bull. 38, 277–282.
Kalivas, P. W., Miller, J. S. (1984) Substance P modulation of dopamine in the nucleus accumbens. Neurosci. Lett. 48, 55–59.
Kanazawa, I., Jessell, T. (1976) Post mortem changes and regional distribution of substance P in the rat and mouse nervous system. Brain Res. 117, 362–367.
Kemble, E. D., Tapp, J. T. (1968) Passive and active avoidance performance following small amygdaloid lesions in rats. Physiol. Behav. 3, 713–718.
Kertes, E., Lénárd, L., Nagyházi, G. (1998) The role of substance P in passive avoidance learning and positive reinforcement. Neurobiology 6, 212.
Kosaka, K., Hama, K., Nagatsu, I., Wu, J. Y., Kosaka, T. (1988) Possible coexistence of amino acid (γ-aminobutyric acid), amine (dopamine) and peptide (substance P): neurons containing immunore-activities for glutamic acid decarboxylase, tyrosine hydroxylase and substance P in the hamster main olfactory bulb. Exp. Brain Res. 71, 633–642.
Krappman, P., Hasenöhrl, R. U., Frisch, C., Huston, H. P. (1994) Self-administration of neurokinin substance P into the ventromedial caudate-putamen in rats. Neuroscience 62, 1093–1101.
Liang, K. C., McGaugh, J. L., Martinez, J. L., Jensen, R. A., Vasquez, B. J., Messing, R. B. (1982) Post-training amygdaloid lesions impair retention of an inhibitory avoidance response. Behav. Brain Res. 4, 237–249.
Ljungdahl, A. T., Hökfelt, G., Nilsson, G., Goldstein, M. (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat. II. Light microscopic localization in relation to catecholamine-containing neurons. Neuroscience 3, 945–976.
Maneo, H., Kyama, H., Tohyama, M. (1993) Distribution of the substance P receptor (NK-1 receptor) in the central nervous system. Mol. Brain Res. 18, 43–58.
Nagel, J. A., Huston, J. P. (1988) Enhanced inhibitory avoidance learning produced by post-trial injections of substance P into the basal forebrain. Behav. Neural Biol. 49, 374–385.
Nagel, J. A., Kemble, E. D. (1976) Effects of amygdaloid lesions on the performance of rats in four passive avoidance tasks. Physiol. Behav. 17, 245–250.
Nicoll, R., Schrenker, C., Leeman, L. (1980) Substance P as a transmitter candidate. Annu. Rev. Neurosci. 3, 227–268.
Pellegrino, L. J., Pellegrino, A. S., Cushman, A. J. (1979). A Stereotaxic Atlas of the Rat Brain. Plenum Press, New York and London.
Pickel, V. M., Joh, T. H., Chan, J. (1988) Substance P in the rat nucleus accumbens: ultrastructural localization in axon terminals and their relation to dopaminergic afferents. Brain Res. 444, 247–264.
Roberts, G. W., Woodhams, P. L., Polak, J. M., Crow, T. J. (1982) Distribution of neuropeptides in the limbic system of the rats: The amygdaloid complex. Neuroscience 7, 99–131.
Sakanaka, M., Shiosaka, S., Takatsuki, K., Inagaki, S., Takagi, H., Senba, E., Kawai, Y., Matsuzaki, T., Tohyama, M. (1981) Experimental immunohistochemical studies on the amygdalofugal peptider-gic (substance P and somatostatin) fibers in the stria terminalis of the rat. Brain Res. 221, 231–242.
Sanberg, B., Iversen, L. (1982) Substance P. J. Med. Chem. 25, 1009–1015.
Sarter, M., Markowitsch, H. J. (1985) Involvement of the amygdala in learning and memory: A critical review, with emphasis on anatomical relations. Behav. Neurosci. 99, 342–380.
Schildein, S., Agmo, A., Huston, J. P., Schwarting, R. K. W. (1998) Intraaccumbens injections of substance P, morphine and amphetamine: effects of conditioned place preference and behavioural activity. Brain Res. 790, 185–194.
Schlesinger, K., Lipsits, D., Peck, P., Pelleymounter, M., Stewart, J., Chase, T. (1983) Substance P enhancement of passive and active avoidance conditioning in mice. Pharmacol. Biochem. Behav. 19, 655–661.
Staubli, U., Huston, J. P. (1985) Central action of substance P: Possible role in reward. Behav. Neural Biol. 43, 100–108.
Treptow, K., Oehme, P., Gabler, E., Bienert, M. (1983) Modulation of locomotor activity by substance P in rats. Reg. Peptides 5, 343–351.
Author information
Authors and Affiliations
Corresponding author
Additional information
Dedicated to Professor József Hámori on the occasion of his 70th birthday.
Rights and permissions
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Lénárd, L., Kertes, E. Influence of Passive Avoidance Learning by Substance P in the Basolateral Amygdala. BIOLOGIA FUTURA 53, 95–104 (2002). https://doi.org/10.1556/ABiol.53.2002.1-2.11
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1556/ABiol.53.2002.1-2.11