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Amygdalostriatal Projections in Reptiles: a Tract-Tracing Study in the Lizard Podarcis Hispanica

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Amygdalostriatal Projections in Reptiles: a Tract-Tracing Study in the Lizard Podarcis Hispanica THE JOURNAL OF COMPARATIVE NEUROLOGY 479:287–308 (2004) Amygdalostriatal Projections in Reptiles: A Tract-Tracing Study in the Lizard Podarcis hispanica AMPARO NOVEJARQUE,1 ENRIQUE LANUZA,2 AND FERNANDO MARTI´NEZ-GARCI´A1* 1Departament de Biologia Funcional i Antropologia Fı´sica, Facultat de Cie`ncies Biolo`giques, Universitat de Vale`ncia, ES-46100 Vale`ncia, Spain 2Departament de Biologia Cellular, Facultat de Cie`ncies Biolo`giques, Universitat de Vale`ncia, ES-46100 Vale`ncia, Spain ABSTRACT Whereas the lacertilian anterior dorsal ventricular ridge contains unimodal sensory areas, its posterior part (PDVR) is an associative center that projects to the hypothalamus, thus being comparable to the amygdaloid formation. To further understand the organization of the reptilian cerebral hemispheres, we have used anterograde and retrograde tracing techniques to study the projections from the PDVR and adjoining areas (dorsolateral amyg- dala, DLA; deep lateral cortex, dLC; nucleus sphericus, NS) to the striatum in the lizard Podarcis hispanica. This information is complemented with a detailed description of the organization of the basal telencephalon of Podarcis. The caudal aspect of the dorsal ventric- ular ridge projects nontopographically mainly (but not exclusively) to the ventral striatum. The NS projects bilaterally (with strong ipsilateral dominance) to the nucleus accumbens, thus recalling the posteromedial cortical amygdala of mammals. The PDVR (especially its lateral aspect) and the dLC project massively to a continuum of structures connecting the striatoamygdaloid transition area (SAT) and the nucleus accumbens (rostrally), the projec- tion arising from the dLC being probably bilateral. Finally, the DLA projects massively and bilaterally to both the ventral and dorsal striatum, including the SAT. Our findings lend further support to the view that the PDVR and neighboring structures constitute the reptil- ian basolateral amygdala and indicate that an emotional brain was already present in the ancestral amniote. These results are important to understand the comparative significance of the caudal aspect of the amniote cerebral hemispheres, and specifically challenge current views on the nature of the avian caudal neostriatum. J. Comp. Neurol. 479:287–308, 2004. © 2004 Wiley-Liss, Inc. Indexing terms: striatum; reptiles; comparative neuroanatomy; emotional brain The telencephalon of reptiles, like the one of birds, dis- Verkley, 1978; Ulinski, 1983; Bruce and Butler, 1984b). As plays a subventricular structure just dorsal to the stria- a consequence, the DVR was compared with the sensory tum that protrudes into the ventricle, thus known as dorsal ventricular ridge (DVR; see Ulinski, 1983). The comparative significance of this structure, i.e., its counter- part in the mammalian brain, has been the center of a Grant sponsor: Spanish MCyT/FEDER; Grant number: BFI2001-3535; Grant sponsor: Universitat de Vale`ncia, Programa Cinc Segles. long debate (see Lohman and Smeets, 1990; Karten, 1991, *Correspondence to: Fernando Martı´nez-Garcı´a, Departament de Biolo- 1997; Butler, 1994; Striedter, 1997; Kaas and Reiner, gia Funcional i Antropologia Fı´sica (Unitat de Morfologia Microsco`pica), 1999). The use of tract tracing methods in reptiles and Facultat de Cie`ncies Biolo`giques, Universitat de Vale`ncia, C. Dr. Moliner, birds demonstrated that the DVR is the target of ascend- 50, ES-46100, Burjassot, Vale`ncia, Spain. E-mail: fernando.mtnez- [email protected] ing projections from at least three different dorsal tha- Received 20 February 2004; Revised 17 June 2004; Accepted 14 July lamic nuclei usually considered the putative relays of vi- 2004 sual, auditory, and somatosensory information (Karten, DOI 10.1002/cne.20309 1969; Karten et al., 1973; Lohman and van Woerden- Published online in Wiley InterScience (www.interscience.wiley.com). © 2004 WILEY-LISS, INC. 288 A. NOVEJARQUE ET AL. neocortex of mammals or to some neuronal populations The alternative views by Bruce and Neary (1995b) and within it (Karten, 1991; Powers and Reiner, 1993; Butler, Striedter (1997) can be reconciled using hodological data 1994)., in lizards that indicate the presence of two functionally In reptiles, the DVR gives rise to descending projections distinct anteroposterior divisions in the DVR (Lanuza et to the underlying dorsal striatum (Hoogland, 1977; Ulin- al., 1998). The anterior DVR (ADVR), apparently contains ski, 1978; Voneida and Sligar, 1979; Gonza´lez et al., 1990), three unimodal sensory areas (auditory, medial; somato- which are commonly seen as the link between the telen- sensory, intermediate; visual, lateral; see Ulinski, 1983), cephalic sensory centers and the motor system, thus me- whereas the posterior DVR (PDVR) seems to be an asso- diating sensorimotor integration (see Ulinski, 1983). In ciative structure that receives convergent projections from line with the data on the thalamic afferents, these projec- the three sensory fields of the ADVR (Andreu et al., 1996; tions were interpreted as equivalent to the corticostriatal Lanuza et al, 1998). The intratelencephalic and extrate- circuits of the mammalian brain. lencephalic afferents of the PDVR (Belekhova and Chk- Recent data on the development, topology, connections, heidze, 1991, 1992; Andreu et al, 1996; Lanuza et al., and expression of homeotic genes in the telencephalon of 1998) together with its projections to the hypothalamus mammals and nonmammalian amniotes have seriously (Bruce and Neary, 1995a; Lanuza et al., 1997; Martı´nez- challenged this view. First, studies on the expression of Marcos et al., 1999) strongly suggest that the PDVR is homeotic genes during development (Smith-Ferna´ndez et part of the reptilian basolateral amygdala. al., 1998; Puelles et al., 2000) indicate that the DVR is not In view of this parcellation of the reptilian DVR, the homologous to the neocortex but to parts of the lateral extent and significance of the projections from the DVR to pallium (piriform and/or endopiriform) plus a region just the basal ganglia needs to be reassessed. The aim of the ventral to it and dorsal to the striatum. This area, which present study is to characterize the striatal projections of has been called ventral pallium (Puelles et al., 2000), the caudal aspect of the dorsal ventricular ridge in the Old apparently composes parts of the mammalian claus- World lizard Podarcis hispanica. To do so, we have first troamygdaloid complex, including the ventral endopiri- studied the cyto- and chemoarchitecture of the basal fore- form area and parts of the basolateral amygdala. This brain of Podarcis. Then, we have analyzed the antero- interpretation partially agrees with the hypothesis by grade transport resulting from tracer injections in the Bruce and Neary (Bruce and Neary, 1995b), according to PDVR and adjacent areas, as well as the retrograde label- which the reptilian DVR is comparable to the lateral ing after tracer injections in the basal ganglia. The results amygdala of mammals. An alternative hypothesis, which of these experiments indicate the presence of important also fits partially the data of expression of homeotic genes, projections from the putative basolateral amygdala was already put forward by Holmgren (1925) and has been (PDVR and adjacent structures) to different parts of the revisited recently by Striedter (1997), who proposed that striatum, including the nucleus accumbens, which would the DVR of the sauropsidian forebrain is comparable to be equivalent to the amygdalostriatal projections present the mammalian claustroendopiriform complex. in the mammalian telencephalon. These findings have Abbreviations ABC avidin–biotin complex Nac nucleus of the anterior commissure ac anterior commissure Naot nucleus of the accessory olfactory tract Acb nucleus accumbens Nmfb bed nucleus of the medial forebrain bundle AChase acetyl cholinesterase NS nucleus sphericus ADVR anterior dorsal ventricular ridge OT olfactory tubercle AONv ventral anterior olfactory nucleus PAP peroxidase–antiperoxidase method aot accessory olfactory tract PB phosphate buffer BDA biotinylated dextran amine PDVR posterior dorsal ventricular ridge BST bed nucleus of the stria terminalis PHA-L Phaseolus vulgaris leucoagglutinin BSTl bed nucleus of the stria terminalis, lateral PT pallial thickening BSTm bed nucleus of the stria terminalis, medial PVA periventricular area Љ DAB 3,3 -diaminobenzidine RDA tetramethylrhodamine-labeled dextran amine DBN diagonal band nucleus RC retrochiasmatic area DBNh diagonal band nucleus, horizontal limb S septum DBNv diagonal band nucleus, vertical limb SAT striatoamygdaloid transition area DC dorsal cortex SATl striatoamygdaloid transition area, lateral aspect DLA dorsolateral amygdaloid nucleus SATm striatoamygdaloid transition area, medial aspect dLC deep lateral cortex Si nucleus septalis impar DSt dorsal striatum DVR dorsal ventricular ridge sm stria medullaris GP globus pallidus SO supraoptic nucleus HRP horseradish peroxidase SP substance P LA lateral amygdala St striatum proper LC lateral cortex st stria terminalis lfb lateral forebrain bundle TB Tris buffer LHA lateral hypothalamic area TBS Tris-buffered saline lot lateral olfactory tract TH tyrosine hydroxylase MA medial amygdala VAA ventral anterior amygdala MC medial cortex VP ventral pallidum mfb medial forebrain bundle VPA ventral posterior amygdala MPA medial preoptic area zl zona limitans MPO medial preoptic nucleus AMYGDALOSTRIATAL PROJECTIONS IN LIZARDS 289 important implications for the understanding of
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