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Afferent Connections to the Striatum and the Nucleus Accumbens

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Afferent Connections to the Striatum and the Nucleus Accumbens THE JOURNAL OF COMPARATIVE NEUROLOGY 378:16–49 (1997) Basal Ganglia Organization in Amphibians: Afferent Connections to the Striatum and the Nucleus Accumbens OSCAR MARI´N,1 AGUSTI´N GONZA´ LEZ,1* AND WILHELMUS J.A.J. SMEETS2 1Departamento de Biologı´a Celular, Facultad de Biologı´a, Universidad Complutense, Madrid, Spain 2 Graduate School of Neurosciences of Amsterdam, Research Institute of Neurosciences and Department of Anatomy and Embryology, Vrije Universiteit, Amsterdam, The Netherlands ABSTRACT As part of a research program to determine if the organization of basal ganglia (BG) of amphibians is homologous to that of amniotes, the afferent connections of the BG in the anurans Xenopus laevis and Rana perezi and the urodele Pleurodeles waltl were investigated with sensitive tract-tracing techniques. Hodological evidence is presented that supports a division of the amphibian BG into a nucleus accumbens and a striatum. Both structures have inputs in common from the olfactory bulb, medial pallium, striatopallial transition area, preoptic area, ventral thalamus, ventral hypothalamic nucleus, posterior tubercle, several mesencephalic and rhombencephalic reticular nuclei, locus coeruleus, raphe, and the nucleus of the solitary tract. Several nuclei that project to both subdivisions of the BG, however, show a clear preference for either the striatum (lateral amygdala, parabrachial nucleus) or the nucleus accumbens (medial amygdala, ventral midbrain tegmentum). In addition, the anterior entopeduncular nucleus, central thalamic nucleus, anterior and posteroventral divisions of the lateral thalamic nucleus, and torus semicircularis project exclusively to the striatum, whereas the anterior thalamic nucleus, anteroventral, and anterodorsal tegmental nuclei provide inputs solely to the nucleus accumbens. Apart from this subdivision of the basal forebrain, the results of the present study have revealed more elaborate patterns of afferent projections to the BG of amphibians than previously thought. Moreover, regional differences within the striatum and the nucleus accumbens were demonstrated, suggesting the existence of functional subdivisions. The present study has revealed that the organization of the afferent connections to the BG in amphibians is basically similar to that of amniotes. According to their afferent connections, the striatum and the nucleus accumbens of amphib- ians may play a key role in processing olfactory, visual, auditory, lateral line, and visceral information. However, contrary to the situation in amniotes, only a minor involvement of pallial structures on the BG functions is present in amphibians. J. Comp. Neurol. 378:16–49, 1997. r 1997 Wiley-Liss, Inc. Indexing terms: forebrain; solitary tract nucleus; locus coeruleus; visceral; evolution Research during the last two decades has revealed many share numerous cytoarchitectonical and neurochemical similarities in the organization of the basal ganglia (BG) features but differ, to some extent, in the information among reptiles, birds, and mammals (see, e.g., Reiner et precessed and connectivity. The dorsal striatum is consti- al., 1984; Gonza´lez et al., 1990; Reiner and Anderson, 1990; Anderson and Reiner, 1991; Heimer et al., 1991; Smeets, 1992; Zahm and Brog, 1992). One intriguing Contract grant sponsor: Spanish DGICYT; Contract grant number: question is whether this basic organization holds also for PB93-0083; Contract grant sponsor: ENP-STF; Contract grant sponsor: anamniotes, in particular amphibians. The first issue we Spanish FPU; Contract grant sponsor: N Collaborative Grant; Contract want to address is the differentiation of the striatal grant number: CRG-910970. *Correspondence to: Dr. Agustı´n Gonza´lez, Departamento de Biologı´a complex of amphibians into a nucleus accumbens and a Celular, Facultad de Biologı´a, Universidad Complutense, 28040 Madrid, striatum. In mammals, the striatum is formed by two Spain. E-mail: [email protected] major divisions, i.e., dorsal and ventral striatum, which Received 25 March 1996; Revised 9 July 1996; Accepted 9 July 1996 r 1997 WILEY-LISS, INC. AMPHIBIAN BASAL GANGLIA AFFERENTS 17 tuted by the main part of the caudate-putamen, whereas Recently, a new generation of tracers has been intro- the olfactory tubercle and the nucleus accumbens repre- duced, viz. dextran amines (Glover et al., 1986; Fritzsch sent the major components of the ventral striatum (Hei- and Sonntag, 1991; Fritzsch, 1993). These tracers, which mer et al., 1995). By means of cytoarchitectonic criteria, a are transported anterogradely as well as retrogradely, can striatum and a nucleus accumbens were already recog- be delivered to restricted sites in the brain, and are nized in anurans at the beginning of this century (for sensitive enough to enable a selective study of the connec- review, see Northcutt and Kicliter, 1980; Parent, 1986). tions of the striatum and the nucleus accumbens. The Thus, the striatum (caudado-putamen in mammals) occu- main goal of the present study was to get detailed informa- pies the ventrolateral portion of the telencephalic hemi- tion of the afferent connections of the BG in anurans and sphere, whereas the nucleus accumbens lies in the ventro- urodeles. Although the outcome of the present study is medial portion of the telencephalic wall. Further, the partly confirmatory, it makes a substantial contribution to amphibian striatum has been subdivided on the basis of our current understanding of BG organization in amphib- differences in cell density and degree of cell migration into ians for the following reasons: 1) the present study reveals dorsal and ventral parts (Northcutt, 1974). Therefore, the differences in afferent connections between the nucleus terms ‘‘dorsal and ventral striatum’’ used for amphibians accumbens and the striatum in both groups of amphibians; are not equivalent to those employed for mammals. 2) it provides evidence for the existence of a nucleus Despite the early recognition of the amphibian striatum accumbens in the brain of urodeles, which has remained and nucleus accumbens as two anatomically and, most likely, functionally distinct basal forebrain structures, unclear until now; 3) the results also indicate the existence little effort has been made to study each of these structures of regional differences within the striatum and the nucleus separately. A major reason for the lack of such information accumbens; and 4) several afferents to the striatum and may have been the absence of sensitive neuronal tracers the nucleus accumbens are demonstrated, which were not that can be injected at restricted sites. Thus, our current described previously. understanding of BG connections in amphibians is primar- The present study is a first step in a research program ily based on the results of anterograde tracing studies by that aims to answer the question to what extent the BG means of the degeneration technique and, less frequently, organization of amphibians is comparable to that of amni- autoradiography (for reviews, see Northcutt and Kicliter, otes. To reach that goal, hodological, chemoarchitectonical, 1980; Parent, 1986), physiological studies (Vesselkin et al., and developmental aspects of the basal forebrain in am- 1971; Vesselkin and Kovacevic, 1973; Gruberg and Am- phibians are considered. Our accompanying paper deals in bros, 1974; Mudry and Capranica, 1980), or retrograde detail with the sites of origin of the catecholaminergic tracing studies with horseradish peroxidase (Kicliter, 1979; input to the nucleus accumbens and the striatum as Vesselkin et al., 1980; Wilczynski and Northcutt, 1983a; revealed by a combined tract-tracing/transmitter-immuno- Neary, 1988; Wicht and Himstedt, 1988, 1990; Dube´ et al., histochemical study. Further studies will provide informa- 1990). tion on the efferent connections and chemoarchitectonic Abbreviations A anterior thalamic nucleus nri nucleus reticularis isthmi Acc nucleus accumbens Nsol nucleus of the solitary tract Ad nucleus anterodorsalis tegmenti n V nervus trigeminus Aob accessory olfactory bulb n VII nervus facialis Apl amygdala, pars lateralis n VIII nervus octavus Apm amygdala. pars medialis n IX-X glossopharyngeal and vagus nerves Av nucleus anteroventralis tegmenti ob olfactory bulb C central thalamic nucleus P posterior thalamic nucleus Cb cerebellum Pb parabrachial nucleus cStr caudal subdivision of the striatum POa anterior preoptic area DB diagonal band nucleus Ra raphe nuclei Dp dorsal pallium Ri nucleus reticularis inferior dStr dorsal subdivision of the striatum Rm nucleus reticularis medius Ea anterior entopeduncular nucleus Rs nucleus reticularis superior epl external plexiform layer rStr rostral subdivision of the striatum gr granule cell layer of the olfactory bulb SC nucleus suprachiasmaticus gl glomerular layer of the olfactory bulb SIR superficial isthmal reticular nucleus Hab habenula sol solitary tract Ip nucleus interpeduncularis spta striatopallial transition area La lateral thalamic nucleus, anterior division Str striatum Lc locus coeruleus tect tectum mesencephali lfb lateral forebrain bundle Tor torus semicircularis Ll lateral line lobe TP tuberculum posterius Lp lateral pallium v ventricle Lpv lateral thalamic nucleus, posteroventral division Vds tractus descendens nervi trigemini Ls lateral septum VH ventral hypothalamic nucleus m medial tegmental area VM ventromedial thalamic nucleus mfb medial forebrain bundle VL ventrolateral thalamic nucleus ml mitral cell layer of the olfactory bulb Vm nucleus motoris nervi trigemini
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