Behavioural characterization of the core and the shell subregions of the nucleus accumbens in rats
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1 Research Collection Doctoral Thesis Behavioural characterization of the core and the shell subregions of the nucleus accumbens in rats Author(s): Pothuizen, Helena Huberta Johanna Publication Date: 2005 Permanent Link: Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 Diss. ETH No Behavioural characterization of the core and the shell subregions of the nucleus accumbens in rats A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY ZURICH for the degree of Doctor of Natural Sciences presented by HELENA HUBERTA JOHANNA POTHUIZEN Master in science (M. Sc), Vrije Universiteit Amsterdam (NL) born December 7 th, 1976 citizen of The Netherlands accepted on the recommendation of: Prof. Dr. Joram Feldon, examiner Prof. Dr. Georges Di Scala, co-examiner Dr. Benjamin K. Yee, co-examiner 2005
3 Summary The nucleus accumbens, part of the ventral striatum, is located in the forebrain of the rat. It is a heterogeneous structure. Numerous neuroanatomical, neurochemical and neurophysiological findings indicate that it can be partitioned into at least two different subregions: a centrally located core and a peripheral shell. Based on these clear distinctions, it can be suggested that the two accumbal subregions are part of functionally segregated circuits. The present thesis aimed to further characterize behaviourally the core and the shell subregions and to provide evidence for a functional dissociation between the two subregions. To this end, the efficacy of pharmacological temporary inactivation and excitotoxic permanent lesions of either the core or the shell subregion were evaluated on a number of behavioural paradigms known to be mediated by the nucleus accumbens. The results presented in this thesis confirm to existing evidence of a behavioural dissociation between the core and the shell subregions. The core, but not the shell, subregion was demonstrated to be preferentially involved in the regulation of locomotor activity and sensorimotor gating assessed with prepulse inhibition of the acoustic startle reflex. A closer evaluation of the neuropharmacological mechanisms via which the core subregion exerts its preferential effects on prepulse inhibition revealed that it does so via glutamatergic rather than dopaminergic substrates. In contrast, the shell subregion was shown to play a pivotal role in the expression of a form of salient learning called latent inhibition. However, the efficacy of shell lesions to affect this behavioural phenomenon appeared to depend largely on the experimental learning paradigm employed. Concurrently, the present findings indicated that the core and shell subregions can be dissociated with respect to their involvement in impulsive behaviour, a functional segregation which had not been established hitherto. The core, but not the shell, subregion was shown to be involved in the control of choice behaviour under delayed reward conditions and in inhibitory control of goal-directed behaviour. Furthermore, novel data was presented which indicate that core- as well as shell-lesioned subjects exhibited facilitated response extinction when tested on an appetitive instrumental conditioning paradigm in comparison to control subjects. Thus, in contrast to the clear aforementioned functional segregations, the core and the shell both contribute to the control of extinction learning of appetitively motivated behaviour. Finally, the efficacy of partial and complete excitotoxic hippocampal lesions on a spatial learning paradigm known to be sensitive to shell lesions was investigated. Again a functional 13
4 Summary segregation was established; the dorsal, but not the ventral, hippocampus was preferentially involved in performance of this task. However, these results concomitantly imply that in some cases functional differences cannot be easily mapped onto differences in anatomical connection patterns Taken together, the findings presented in this thesis clearly indicate that the core and the shell indeed are part of functionally segregated circuits. Part of the present data concur with the notion that the shell subregion is primarily involved in the attribution of motivational valence to stimuli, whereas the core plays a role in the motor expression of motivated or conditioning-dependent behaviour. However, the present data also indicate that the current theories might have to be extended to accommodate these novel findings. 14
5 Zusammenfassung Der Nucleus Accumbens, der ein Teil des ventralen Striatums ist, liegt bei der Ratte im Vorderhirn und stellt eine heterogene Struktur dar. Zahlreiche neuroanatomische, neurochemische und neurophysiologische Forschungsergebnisse deuten darauf hin, dass er in mindestens zwei verschiedene Subregionen unterteilt werden kann: nämlich eine zentral gelegene Core und eine mehr peripher gelegene Shell Subegion. Basierend auf dieser klaren Unterscheidung kann angenommen werden, dass die zwei Subregionen des Nucleus Accumbens Teil von funktional getrennten (unterschiedlichen) Hirnschaltkreisen sind. Das Ziel dieser Dissertation ist eine weiterführende Charakterisierung der Core und der Shell Subregion des Nucleus Accumbens in Bezug auf das Verhalten der Ratte und der Nachweis einer funktionellen Abgrenzung dieser zwei Subregionen. In den hier vorgestellten Studien wurden die Wirksamkeiten pharmakologischer temporärer Inaktivierung und permanenter, durch Zelltod induzierte (excitotoxische) Läsion der Core oder der Shell Subregion in einer Anzahl von Verhaltensparadigmen beurteilt, bei welchen eine Beteiligung des Nucleus Accumbens bekannt ist. Die in dieser Dissertation vorgestellten Resultate bestätigen die schon existierenden Hinweise einer Verhaltensabgrenzung zwischen der Core und der Shell Subregion des Nucleus Accumbens. Es ist gezeigt worden, dass die Core, nicht aber die Shell Subregion, vor allem an der Regulation lokomotorischer Aktivität und sensomotorischer Filterung, welche durch Prepuls Inhibition des akustischen Schreckreflexes gemessen wird, beteiligt ist. Eine genauere Untersuchung der neuropharmakologischen Mechanismen, durch welche die Core Subregion ihren bevorzugten Effekt auf Prepuls Inhibition hat, zeigte, dass dies eher durch glutamaterge als durch dopaminerge Substrate geschieht. Im Gegensatz dazu wurde gezeigt, dass die Shell Subregion in der Äusserung einer speziellen Form von assoziativem Lernen, genannt Latente Inhibition, eine entscheidende Rolle spielt. Ob und wie sehr eine Läsion der Shell Subregion dieses Phänomen jedoch beeinflusst, scheint hauptsächlich vom Lernparadigma des Experiments abzuhängen. Zudem deuten die hier vorgestellten Resultate an, dass die Core und die Shell Subregionen in Bezug auf ihre Beteiligung bei impulsivem Verhalten unterschieden werden können. Diese funktionale Teilung der beiden Subregionen wurde bis jetzt noch nicht nachgewiesen. Es wurde gezeigt, dass die Core Region, nicht aber die Shell Region, in der Kontrolle von Auswahlverhalten bei verzögerten Belohnungen und in zielgerichtetem Verhalten beteiligt ist. Im Weiteren wurden neue Daten gezeigt die darauf hindeuten, dass im 15
6 Zusammenfassung Vergleich zu Tieren ohne Läsion solche mit Läsion der Core oder der Shell Subregion eine erleichterte Auslöschung der Verhaltensantwort in einem appetitiven instrumentellen Konditionierungsparadigma zeigen. Somit konnte bewiesen werden, dass die Core und die Shell Subregionen zur Kontrolle des Auslöschungslernens bei appetitiv motiviertem Verhalten beitragen, dies im Gegensatz zu den vorher genannten, klar unterschiedlichen Funktionen beider Subregionen. Zu guter Letzt wurde auch die Wirkung von vollständigen oder partiellen excitotoxischen Läsionen des Hippocampus untersucht und zwar in Bezug auf ein räumliches Lernparadigma, das erwiesenermassen sensitiv für Läsionen der Shell Subregion des Nucleus Accumbens ist. Erneut wurde eine funktionale Trennung gefunden; vor allem der dorsale, nicht aber der ventrale Hippocampus war beim Lösen der räumlichen Aufgabe beteiligt. Dennoch, diese Resultate schliessen begleitend ein, dass sich in manchen Fällen funktionale Unterschiede nicht einfach auf unterschiedliche anatomische Verbindungswege zurückführen lassen. Zusammengefasst zeigen die in dieser Dissertation vorgestellten Forschungsergebnisse, dass die Core und die Shell Subregionen des Nucleus Accumbens in der Tat Teile funktional verschiedener Hirnschaltkreise sind. Ein Teil der Daten stimmt mit der in der Fachliteratur vorherrschenden Meinung überein, dass die Shell Subregion vor allem an der Zuordnung des Motivationswertes eines Stimulus beteiligt ist. Die Core Subregion auf der anderen Seite ist an der motorischen Äusserung von motiviertem oder konditioniertem Verhalten beteiligt. Die hier vorgestellten Daten zeigen aber auch, dass aktuelle Theorien angepasst werden müssten, um diesen neuen Erkenntnissen Rechnung zu tragen. 16
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