Neurochemical Organization of the Turtle Pretectum - Springer Link

Journal of Evolutionary Biochemistry and Physiology, Vol. 38, No. 6, 2002, pp. 673—688. Translated from Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, Vol. 38, No. 6, 2002, pp. 530—542. Original Russian Text Copyright © 2002 by Kenigfest, Belekhova, Karamyan, Minakova, Rio, Repérant.

REVIEWS

Neurochemical Organization of the Turtle Pretectum: An Immunohistochemical Study. Comparative Analysis N. B. Kenigfest*, ***, M. G. Belekhova*, O. A. Karamyan*, M. N. Minakova*, J.-P. Rio**, and J. Repérant *** * Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences,

St. Petersburg, Russia ** Institute of National Health and Medical Investigations INSERM U-106, Paris, France *** National Museum of Natural History, Paris, France Received February 8, 2002

Abstract—A comparative analysis of neurochemical organization of pretectal nuclei was performed on the basis of results of our studies on immunoreactivity to monoamines (tyrosine hydroxylase—TH and serotonin—5-HT), neuropeptides (substance P—SP, met-enkephalin—mEnk, and neuropeptide Y, NPY), and gamma-aminobutyric acid (GABA) in pretectum of two turtle species, as well as of the corresponding literature data obtained in other reptile species, birds, and mammals. Their presumed homologous pretectal nuclei were shown to have both similar and different immunohistochemical features. A conclusion is made that species of divergent lines of amniotes have not only the evolutionary conservatism of the neurochemical organization of pretectal structures and their projection pathways but also its certain plasticity due to rearrangements in the course of phylogenetic development.

INTRODUCTION Pretectum, unlike other subtelencephalic structures, is poorly studied in comparative investigations of amniotic brain. Up to now the boundary between pretectum and caudal thalamus in reptiles has remained a subject of discussion [1]. Even more complicated are their interrelations in representatives of lower vertebrates [2]. Connections of pretectum in reptiles were studied mostly within the visual system [3–8] or in terms of its relationships with pallido-mesencephalic motor [9–11] and optico-autonomous [12–14] systems. Although the available, rather incomplete data on the pretectum organization in reptiles and birds have allowed suggesting homology of some pretectal nuclei in amniotes [5, 7, 8, 15–20], they are certainly insufficient to consider the problem solved. Studies

of neurochemical characteristics of brain structures in phylogenesis and embryogenesis in terms of neuromeric segmentation have made it possible to trace more reliably succession of their development in the course of evolution [20–24]. Thus, there were described functional brain systems with identical neurochemical characteristics, which show high evolutionary conservatism at least in amniotes [9, 10, 19, 21–23]. However, the equivalent and as a whole phylogenetically conservative brain systems, such as the monoaminergic system, have a marked variability of he projection distribution not only between different vertebrates classes, but also within the same class, including reptiles [20–23, 25–27]. These data raise the question as to developmental plasticity of the transmitter–modulator systems of the brain in the course of vertebrate evolution. The goal of the present study is a comparative anal-

0022-0930/02/3806-0673$27.00 © 2002 MAIK “Nauka/Interperiodica”

674

KENIGFEST et al.

ysis of neurochemical organization of amniotic pretectum on the basis of our own immunohistochemical data (turtles) and similar literature data (other reptile species, birds, and mammals). Studied in turtle pretectal nuclei was immunohistochemical distribution of immunoreactivity (IR) to serotonin (5-HT), tyrosine hydroxylase (TH), an enzyme involved in synthesis of dopamine (DA)1, neuropeptides (substance P, SP; met-enkephalin, mEnk; neuropeptide Y, NPY), and gamma-aminobutyric acid (GABA) to check similarity of these neurochemical characteristics among the assumed homologues of amniotic pretectal nuclei. MATERIALS AND METHODS The study was carried out on 32 turtles Testudo horsfieldi (n = 21) and Emys orbicularis (n = 11). The animals under deep Nembutal anesthesia (40–60 mg/kg) were transcardially perfused first with 0.7% NaCl added with heparin and then with a fixative solution containing either 4% paraformaldehyde and 0.4 % glutaraldehyde (for study of distribution of 5-HT, TH, and SP) or 1% paraformaldehyde and 1.25% glutaraldehyde (in the case of GABA) in 0.1 M phosphate buffer, pH 7.4. The extirpated brain was postfixed in the same solution and allowed to stay overnight in 20– 30% sucrose in 0.1 M phosphate buffer. Immunohistochemical reaction was performed in freely floating, 25–50-µm thick sections cut on a freezing microtome. After inhibition of endogenous peroxidase activity in 1% H2O2 and inhibition of unspecific antibody binding in 2–3% normal goat serum the sections were incubated for 15–17 h at room temperature with polyclonal antibodies obtained in rabbits against 5-HT (Immunotech, France) diluted 1:1000; against TH (Jean Thilbault, France), 1 : 1000; against SP and NPY (Peninsula Lab., USA), 1 : 500–1 : 1000; against mEnk (Chemicon, USA), 1:1000; and against GABA (Immunotech, France), 1:2000. The sections were washed out in several changes of the buffered (0.05 M Tris buffer, pH 7.6) saline and incubated for 1 h at

1 We did not perform special experiments with use of dopam-

ine-β-hydroxylase (DBH) to differentiate DA- and noradrenaline-immunoreactivity. Based on data of works [20, 27] demonstrating the predominant coincidence of immunoreactivity to TH and to DA in the reptile brain, we considered the TH-IR structures as DA-containing.

room temperature in biotinated goat anti-rabbit serum (Vectastain, USA) diluted 1 : 200. The buffered saline containing 0.03–0.1% Triton X-100 and 1–3% normal goat serum was used as a solvent for primary and secondary antibodies. After washing out, the sections were incubated for 1 h with avidin-biotin-conjugated horseradish peroxidase (HRP) (ABC, Vectastain, USA) diluted 1 : 50–1 : 100 in the buffered saline containing 0.1% Triton. The HRP activity was visualized in 0.03% diaminobenzidine (Sigma, USA) with added 0.01% H2O2 in 0.05 M Tris buffer, pH 7.6. In control experiments, with replacement of primary antibodies with the equivalent amount of normal goat serum, the complete absence of immune reaction was observed. The material was examined in a light microscope, density of immunoreactivity and the amount of immunoreactive neuronal bodies were evaluated, and their maximal diameter was measured using an ocular micrometer. To describe the turtle brain structures, the most common nomenclature was used [3, 4, 28]. Abbreviations used in the article: Apr—area pretectalis, CS—colliculus superior, CP—commissura posterior, GC—griseum centrale, Gt—n. griseus tecti, Hab—habenula, Lm—n. lentiformis mesencephali, LP—n. lateralis posterior, nCP—n. commissurae posterior, ndCP—n. dorsalis commissurae posterior, NOL—n. olivaris pretectalis, nOptVL—n. opticus ventrolateralis, NOT—n. tractus opticus, NPA—n. pretectalis anterior, NPL—n. posterior limitans, NPM—n. pretectalis medialis, NPP—n. pretectalis posterior, Pd—n. posterodorsalis, Pedv—pedunculus ventralis fasciculi telencephali lateralis, Po—n. posterior, Pt—n. pretectalis, Ptd—n. pretectalis dorsalis, Ptv—n. pretectalis ventralis, Pulv—pulvinar, Rot—n. rotundus, SGP—stratum griseum periventriculare TO, SPL—n. spiriformis lateralis, SPM—n. spiriformis medialis, Sub/IPS—n. subpretectalis/n. interstitio-pretecto-subpretectalis, TO—tectum opticum, Tro—tractus opticus, Trtth—tractus tectothalamicus. RESULTS Distribution of IR structures was analyzed in retinorecipient (Lm, Gt, Pd, nOptVL) and predominantly non-retinorecipient (Ptd, Ptv, Po, ndCP) nuclei of turtle pretectum. Labeled structures were represented by stained bundles and diffusely scattered fiber fragments with a varying amount of varicosities

JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 38 No. 6 2002

675

NEUROCHEMICAL ORGANIZATION OF THE TURTLE PRETECTUM

TH (a)

5-HT TO

SP (c)

(b)

SGP CP Pd Gt Lm Ptd ndCP Ptv Po GC Trtth Tro

NPY

mEnk (d)

(e)

GABA (f )

Fig. 1. Distribution of monoamine- and neuropeptide-immunoreactive elements in the turtle pretectum. TH, 5-HT, SP, mEnk, NPY, GABA (a)–(f )—scheme of frontal sections at the pretectum level. Black shows immunoreactive neurons, light—weak staining (NPY); dots—terminals, lines—fragments of fibers and fiber bundles. Designations in this and other figures, see in the section “Abbreviations used.”

that can be considered as synaptic and non-synaptic terminals as well as by isolated fine-granular terminal-like structures (called later as terminals). For TH, mEnk, NPY, and GABA, immunopositive neuronal bodies were revealed. Distribution of IR structures in turtle pretectum is shown in averaged (for all cases with each substance) diagrams of brain frontal sections (Fig. 1). Tyrosine hydroxylase (TH). The highest density of IR structures is revealed in Pd (Fig. 1a). Multiple immunopositive cell bodies (up to 20 or more per section) were densely packed in peripheral parts of the nucleus surrounding its rounded core with only oc-

casional cell bodies (Figs. 2a, 2b). Small (9–14.4 µm, the mean 12.5 µm, n = 63) rounded or spindle-like, or more often pyriform and multipolar neurons were predominant (70%). The rest of the neurons (30%) were represented by large (15.6–19.2 µm, the mean 17 µm, n = 27) cells of a similar shape scattered in the nucleus. Most neurons had short dendrites directed towards the core neuropil of Pd, while in some neurons, dendrites rounded the nuclear core without penetrating it (Figs. 1a, 2a, 2b). Ventrally, the IR neurons of Pd were constantly fused with immunopositive cells surrounding the dorsal Ptd pole and with cells located in ndCP and GC. They were predominantly small


676

KENIGFEST et al.

Fig. 2. Tyrosine hydroxylase-immunoreactive elements. (a), (b) Dense IR terminal area in the core of Pd (arrows) and scarcer terminals and IR neurons in the peripheral part of Pd and ndCP. (b) Shows Pd cells with dendrites inserted into its core (sharp arrow) or surrounding it (double arrows). Arrows in (c) show dendrites of ndCP cells inserted into Ptd; scarce terminals are seen in Ptd and their absence Ptv (a), (c). (d) Bipolar IR neurons with dendrites running to Hab and Pd (arrow). Bar scale (µm): (a), (b) 100, (b) 50, (c) 25.

cells (9–14.4 µm, the mean 12.1 µm, n = 91) that had a rounded, pyriform or spindle-like shape. Less common were medium-sized cells (15.6–19.2 µm, the mean 16.8 µm, n = 18). Many neurons had long, poorly branched dendrites extended to and penetrating the adjacent nuclei, Ptd and Ptv (Figs. 2a, 2b). Spindlelike bipolar IR cells were revealed above CP; they had one dendrite directed to Pd, while the other was traced up to Hab (Fig. 2d). Among the IR innervating structures, predominant were fragments of thin fibers with or without varicosities and with scattered among them fine-granular structures. All of them had maximal density in the Pd core; as a result, it looked as a round-

ed, intensively dark mass (Figs. 2a, 2b). Density of IR fibers and terminals in peripheral parts of Pd and other pretectal nuclei (Po, LM, ndCP, GC), except for Ptd and Ptv, varied from moderate to insignificant (Figs. 1a and 2a) even within the same nucleus (Po). Quite insignificant amount of IR fibers and terminals was demonstrated in Ptv and Ptd. In the latter, some fiber fragments most likely belonging to dendrites of IR neurons of ndCP were found to pass the Ptd crosssection (Figs. 1a and 2c). The course of immunopositive fiber bundles rounding GC and diverging radially at the level of ndCP was traced. Practically no IR fibers were present in Trtth and CP, except for the



677

Fig. 3. Serotonin-immunoreactive elements. (a) IR terminals and fibers in the peripheral part of Pd and very scarce in its core (arrows). (b)–(d) Very dense IR terminal area in Ptd, of mild density, in Lm, Po, nOptVL, of low density, in other nuclei. (e)–(g) Various samples of 5HT innervation of Ptd (e), Lm (f ), and Ptv (g). Bar scale (µm): (a), (c), (d), (g) 100, (e), (f ) 25.

dorsal CP portion binding two sides of Pd (Fig. 1a). Serotonin (5-HT). No IR neuronal bodies were revealed in any of the nuclei. Distribution of IR innervating structures in Pd and Ptd differed markedly. In Pd the core part was almost deprived of IR fibers and

terminals, while some of them were found in its peripheral area (Fig. 1b). Like in the case of TH, they were represented by thin varicose fibers and fine-granular terminals (Fig. 3a). On the contrary, in Ptd (Fig. 3b) their very high density was constantly ob-


678

KENIGFEST et al.

Fig. 4. SP-immunoreactive elements. (a) General picture of distribution of IR mainly in nuclei surrounding Ptd and Ptv; (b), (c) terminals and fibers are concentrated in the peripheral part of Pd, they are very rare in the core (arrows). Higher magnification shows (d)–(f ) dense accumulations of IR terminals in Lm (d), Po (e) and in the vicinity of Pd (c), and occasional scattered terminals in Ptd (d) and Ptv (e), (f ); (c) and (e) reveal fragments of fiber bundles (double arrows) in Po (e) and in the vicinity of Pd (c); (d) demonstrates accumulation of IR cells in the tectum. Bar scale (µm): (a) 200, (c) 100, (b), (d)–(f ) 50.

served, as a rule on the background of a yellow staining presumably associated with non-synaptic local-

ization of the substance. Both in Ptv and in Trtth the immunopositive structures occurred much more sel-



679

Fig. 5. Met-enkephalin-immunoreactive elements. (a), (b): Pd—very dense IR area (a), accumulation of IR neurons (b) in the core of the nucleus are shown by arrows; rare terminals and cells (double arrow in (a)) in its peripheral part. (c), (d) IR terminal areas of moderate density in Lm, Po, of significant density with IR neurons (arrow in (d)) inside from Tro and very scarce terminals in Ptd/Ptv. (d), (e) Accumulation of IR neurons in the lower part of ndCP; their processes are directed towards Ptd/ Ptv (arrow in (e)). Bar scale (µm): (a)–(c), (e) 50, (d) 100.

dom (Figs. 1b, 3b, 3c). In Po and Lm nuclei surrounding directly Ptd and Ptv, IR varicose fibers and terminals were distributed relatively uniformly, with a moderate density that decreased in the more distant nuclei (Gt, ndCP) (Figs. 1b, 3b, 3c). At high magnification, differences in innervation pattern of Ptd and other pretectal nuclei were revealed: very thin (as dustlike granules) terminals were predominant in Ptd and Ptv (Figs. 3e, 3g), whereas in other nuclei, for example in Lm, varicose fibers and larger isolated terminals were observed (Fig. 3f ). In two more nuclei, density of IR terminals was significant, but lower than in Ptd. These included nOptVL (n. pretectalis externus, according to [3]), in which small terminals prevailed (Figs. 1b and 3d), and GC containing, apart from ter-

minals, many IR fragments of fibers, especially in the white periventricular layer (Fig. 1b). In CP, IR fibers were scarce, their accumulation being observed in its upper portion. Substance P (SP). No immunopositive cells were revealed in pretectum, although their large amount was observed in the deep, periventricular tectum layer (Figs. 1c and 4d). Practically all the nuclei, except for Ptd and Ptv, contained IR elements in the form of granular structures, much larger than in the case of TH- and 5-HT-IR. Their density was the highest in Po, somewhat lower in Lm and GC, and low in ndCP and Gt. Practically no SP innervation was revealed in Ptd and Ptv with Trtth (Figs. 1c, 4a, 4c–4f ). A dense accumulation of IR terminals was observed in the pe-


680

KENIGFEST et al.

ripheral part of Pd, while its core was almost empty of them (Figs. 4a, 4b). Accumulation of IR structures in CP was traced in its dorsal portion. Dense bundles of intensively stained fibers were found in Pedv and in the tegmentum lateral part. They ran towards pretectum, in which finer bundles were demonstrated around Pd, in its peripheral zone, and in Po (Figs. 1c, 4a, 4c, 4e). Met-enkephalin (mEnk). Several pretectal nuclei were characterized by high IR. The highest density of IR terminals was observed in the core of Pd, while a lower density, in its peripheral part (Figs. 1d and 5a). A solid black staining of the Pd core prevented revealing individual IR structures inside it. However, in some preparations, it was possible to observe accumulation of cells stained more intensively than the terminal area (Fig. 5b). Occasional immunopositive cells were revealed in the peripheral part of the nucleus. In Pd, small neurons (8.4–14.4 µm, the mean 12 µm, n = 22) were predominant (73%). Other neurons were somewhat larger (15.6–18 µm, the mean 16.5 µm, n = 8). All of them varied in shape from rounded to spindle-like. The most abundant population (30 and more per section) of IR cells similar in shape and size to TH-IR neurons was found in ndCP, Po, and GC (Figs. 1d, 5d, 5f). In ndCP, small neurons (10.8– 14.4 µm, the mean 13.9 µm, n = 35) were predominant (more than a half). A half of neurons in Po were middle- and large-sized (15.6–21.6 µm, the mean 18.4 µm, n = 35). A group of neurons were distinguished among IR cells in these nuclei by their long dendrites running towards Ptd and Ptv and penetrating them (Fig. 5e). Another group of predominantly spindle-like cells was oriented in parallel to the course of CP fibers. Small neurons had no definite orientation of the body axis and processes. In the nuclei Lm, Po, nOptVL, and GC, density of IR fibers and terminals was moderate and relatively uniform, while in ndCP and Gt it was significantly lower (Figs. 1d, 5c, 5e). On the contrary, the Ptd–Ptv complex was practically deprived of mEnk innervation. Occasional individual IR fibers found there most likely were fragments of immunopositive cell dendrites located in the adjacent nuclei ndCP and Po (Figs. 1d, 5d, 5e). The course of IR fibers could be followed laterally from Trtth and Pedv, where dense bundles of immunopositive fibers were revealed (Fig. 1d). Neuropeptide Y (NPY ). The general picture of NPY-IR in pretectum of turtles has been published

elsewhere [29]. It also described in detail the NPYIR distribution in each of the pretectal nucleus. IR structures were represented by immunopositive cells and terminals. The varying number (from 5 to 30 per section) of intensively stained neurons was observed in Lm, ndCP, Po, and the peripheral part of Pd. In Ptd they were concentrated mostly at the periphery of the nucleus, where they could be hardly differentiated from IR cells of Lm and Po. Towards the center of Ptd the number of IR neurons and intensity of their staining decreased significantly; in Ptv, they were occasional (Figs. 1e, 6a–6d). Cells in these nuclei were predominantly small (7.8–13.2 µm, the mean 10.8 µm, n = 44) and had a diverse shape—spindlelike, pyriform, or multipolar. Although only proximal cellular processes as a rule were stained, it looked as if they did not leave the boundaries of Ptd and Lm, whereas long dendrites of some neurons in ndCP could be traced to run to Po and Ptd in the same way as those of TH- and mEnk-IR neurons (Figs. 1e, 6c, 6d). Accumulation of IR terminals was observed in Lm and nOptVL; their density in Gt, ndCP, and in the Ptd–Ptv complex was lower (Figs. 1e, 6c, 6d). The NPY-innervation of Pd was similar to the 5-HT- and SP-innervation: its core contained very rare fibers and terminals, while their density in the peripheral part was high (Figs. 1e, 6b, 6e). GC was distinguished by a high amount of IR, especially in the white periventricular layer. In CP, the IR fibers were traced in its dorsal part. Gamma-aminobutyric acid (GABA). Distribution of GABA-IR is presented based on analysis of the material obtained and of data that have been published in part previously [8, 30]. Here we report additional results not published earlier. Figure 1f demonstrates the complete pattern of GABA-IR in pretectum. It had a larger and less selective distribution in various nuclei than TH-, 5-HT-, SP-, and mEnk-IR and overlapped in some nuclei with NPY-IR (Figs. 1e, 1f). Practically all the nuclei had multiple GABA-IR cells with the highest density in Ptv and ndCP (Figs. 1f and 6). Distribution of GABA-IR and NPY-IR neurons in Ptd was similar with respect to their density and localization (primarily, at the periphery of the nucleus). In Ptv, on the contrary, GABA-IR cells filled with a high-density IR-material were uniformly spread in the nucleus, whereas no NPY-IR neurons were present there (Figs. 1f, 6j, 6i). Although localization of GABA-IR and NPY-IR cells in ndCP was similar,



681

Fig. 6. Neuropeptide Y- (a)–(e) and gamma-aminobutyric acid- (f )–( j) immunoreactive elements. (a) General picture of distribution of NPY-IR. (a), (b), (e): Pd—IR terminals are concentrated in the peripheral part of Pd and are very scarce in its core (arrows in (a) and (b)); dendrites of IR cells in the peripheral part of Pd are inserted into its core (arrows in (e)). (a), (c), (d): IR terminals in Pd and Ptv are scarce, in Lm, Po, and ndCP—of moderate density; populations of intensely stained IR neurons in Lm ((a), (c)) and ndCP (d), populations of weakly and densely stained, in Ptd ((a), (c)) (occasional neurons in Ptv). (c), (d) Show processes of IR neurons of ndCP, which pass the Ptd cross section (arrows). (f ), (g): Pd—GABA-IR fibers, terminals, and cells (arrow in (g)) are concentrated in its peripheral part; they are very rare in the core (arrow in (f )). (h) IR neurons in Ptd (they form nuclear capsule) and Ptv (scattered more uniformly). (i), ( j) IR neurons in ndCP, GC, and Ptv; ( j) shows processes of ndCP cells, which are directed towards Ptd/Ptv (arrows). Bar scale (µm): (a), (h), (i) 100, (b)–(g), ( j) 50. JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 38 No. 6 2002

682

KENIGFEST et al.

the number of the former was much higher (Figs. 6d, 6i). In peripheral part of Pd, GABA- and NPY-immunopositive neurons had similar localization (Figs. 6e, 6g). In most cases, bodies and short processes of proximal dendrites of GABA-IR neurons were stained. Therefore, comparison of their morphological characteristics in different pretectal nuclei renders little information. In all the nuclei, except for Ptv, predominant (from 80–90 to 100% in Pd) were small neurons (6–15 µm, n = 44) with mean sizes (µm): 9.8 in Lm, 11.5 in Ptv, 10.8 in Pd, 11.3 in ndCP, 11.6 in Po, and 10 in Pd. Only in Ptv the number of small cells was lower (59%). Large cells (15.6–27 µm, n = 30) were more scarce, except for those in Ptv, and their sizes differed little in different nuclei (µm): 16.4 in Lm, 18.3 in Ptv, 16.8 in ndCP, 16.6 in Ptd, and 16.5 in Po; no such neurons were revealed in Pd. Although neuronal processes were stained rarely and along a short length, attention was paid to that in some cells of ndCP and Po they were directed towards Ptd and Ptv (Fig. 6j) like in TH-, mEnk-, and NPY-IR neurons. Cellular processes in the peripheral part of Pd were directed to its core. Immunopositive terminals also were widely spread in all pretectal nuclei, with the maximal density in retinorecipient nuclei: in the peripheral part of Pd, Lm, nOptVL, along the entire length of optical tract, and in GC. Their density was more moderate in Gt, Po, Ptd, Ptv, and ndCP, while they were practically absent in the core of Pd (Figs. 1f and 6f ). In CP and Trtth, IR fibers were traced. Earlier, we have shown at least a part of pretectal neurons to be projection cells [7, 8]. DISCUSSION To discuss the presumed homology of some pretectal nuclei in amniotes, we pay attention to their essential neurochemical characteristics in reptiles. Unfortunately, comparison with the corresponding characteristics in birds and mammals is extremely difficult due to a strikingly low interest to this brain area in most studies. Review papers on monoamine and neuropeptide immunohistochemistry either ignore pretectum or consider it as the single structure. Papers dealing with study of neurochemical features (NPY, mEnk, Ca-binding proteins) of individual pretectal nuclei have appeared only recently [24, 31–33]. The situation is complicated by the lack of the commonly accepted classification of pretectal nuclei in

amniotes and the partially resulted controversy in evaluation of their connections. The exception are the nuclei that in the complex with accessory optical system nuclei are closely connected with visual-motor functions (see review [34]). Suggestions about homology of some pretectal nuclei in reptiles, birds, and mammals has been made predominantly on the basis of these data [7–10, 15–18]. Below is presented our attempt to find out whether the presumably homologous nuclei of pretectum in amniotes have similar or dissimilar neurochemical characteristics studied in this work and in other studies. Lm (reptiles, birds) and NOT (mammals). Homology of LM of reptiles and birds and mammalian NOT is the best substantiated (see [8]). However, similarity of their neurochemical parameters is far from complete. Their most characteristic common feature of these nuclei is the presence of NPY-IR neurons and terminals, although this is not a unique property of NOT and it varies quantitatively in different mammalian species [31, 33]. Like Lm in turtles (our data, [35]), NOT receives SP-innervation from superior colliculi [36]. However, in the lizard no SP-IR in Lm has been observed [37]. Moreover, this is not a unique feature both of Lm and of NOT. Many pretectal nuclei in mammals contain abundant 5-HT-IR fibers and terminals [32]; however, their maximal density has been described in different nuclei of different species: in the medial NOT part in the rat [38], in NPL and NPM in the hamster [32], in NOL in the cat [32, 39], the latter also having the highest density of 5HT1 receptors [39]. In reptiles (our data, [25, 27, 40– 42]) and birds [43] the 5-HT-IR terminal area of maximal density has been revealed in Ptd and Pt, respectively, but not in Lm. The only exception are snakes, in which it was found in Pd [43]. Lm, like other pretectal nuclei (Po, Pd, Gt) in the turtle and other reptile species, receives essentially less 5-HT innervation than Ptd. A convincing argument in favor of the Lm and NOT homology is the presence in both of them of GABAergic neurons projecting into the lateral geniculate body [8]. On the contrary, the presence of Enk-IR neurons in NOT (its medial part) is in contrast with their absence in Lm of the turtle and the lizard (our data, [26, 47]), even after a pretreatment with colchicine [37]. However, it is to be kept in mind that differences in the number of Enk-IR cells has also been observed in mammals: in cats this nucleus has their maximal amount [31], whereas in rats



their number is rather low and only after a preliminary administration of colchicine and/or after proteolytic treatment of sections [45]. This, Lm in reptiles and birds and NOT in mammals, which have similar connections and functions, are a part of the visual-motor and circadian photo-dependent systems [7, 8, 15, 16, 31, 48] and have both similar and different neurochemical characteristics. Pd/Apr (reptiles, birds) and NOL (mammals). Homology of these nuclei is suggested on the basis of similarity of their connections predominantly with structures of the limbic and circadian systems, specifically with Hab, IGL, suprachiasmatic nucleus, and other hypothalamic nuclei [19, 31, 49–51]. A great similarity between Pd and NOL has been found in their neuronal organization and retinal innervation [4, 28, 52]. Both nuclei are involved in pupillary reflexes (see [53]). However, similarity of their neurochemical characteristics is rather limited. Even ignoring completely pretectum in special papers dealing with distribution of DA/TH-IR in the brain of mammals [54, 55] and birds [56], it was difficult not to notice the presence of dense accumulation of DA/TH-IR neurons and the terminal area in NOL, which are so typical and constant in Pd of turtles ([57], data of the present work) and other reptile species [20, 37, 58– 60]. Based on these data, DA-containing neuronal group in Pd has been suggested to be the common brain feature of all reptiles, which was lost in the course of evolution of mammals [20]. Its precursor can be revealed in some representatives of anamniotes—amphibians and teleost fish—in the form of scattered DAIR cells adjacent to posterior commissure. It has also been described in birds [61, 62], although some other authors [56] have revealed a significant population of DA- and TH-IR neurons in some other pretectal nuclei (NPM, SPM, SPL), rather than in Apr. The fact that the corresponding group of transitory TH-IR neurons has been found at early stage of mammalian embryogenesis in the pretectal neuromere and is lost in adult animals [63] permits considering this to be a manifestation of recapitulation of a character typical of previous stages of vertebrate evolutionary development and lost during transition to mammals. A variable feature of Pd and NOL also is NPY-IR. In some mammals (hamster) the presence of NPYIR cells is a characteristic feature of NOL [31], whereas in others (cat) this is not the case [33]. Among reptiles, small amounts of the NPY-IR neurons have been

683

found in Pd in the turtle (our results) and some lizards [64], and as a dense cluster, in chameleon [65] and in the Pd-comparable nucleus of birds [66]. At the same time, their common feature is NPY innervation. Its source could be neurons of IGL and/or hypothalamus [31]. A close resemblance between these nuclei is seen in the character of Enk-IR. In mammals the presence of Enk- and NPY-IR cells as well as Enk innervation is considered as its specific properties [31]. Pd of turtles and lizards also have Enk-IR neurons and has a peculiar, very dense, Enk-IR-containing terminal area in its core (our data, [47, 67]. A characteristic and common for both Pd and NOL is their abundant SP innervation comparable with TH. It seems to originate from hypothalamus and/or deep layers of tectum, in which we and other authors have revealed many SP-IR neurons in turtles [26, 35] and other reptile species [37, 68]. Like NPY innervation, it is concentrated in peripheral parts of Pd. There are data about close interrelations of the catecholamine and neuropeptide (SP, NPY) systems in vertebrate brain [27]. However, this feature of NOL in mammals also is variable [31, 69]. Thus, although Pd of reptiles, Apr of birds, and NOL of mammals have some similarity in structural and functional organization and are a presumable integration center of visual and motivational information, not all of their neurochemical characteristics are identical. These are variable both in mammals and in sauropsides. Ptv (reptiles) and Sub/IPS (birds); Ptd (reptiles) and Pt (birds). The non-retinorecipient pretectal nucleus in the turtle consists of two independent nuclei Ptv and Ptd combined into the single structure of a peculiar shape, but with different connections and neurochemical characteristics. Hypothesis of homology of the reptilian Ptv and bird Sub/IPS seems quite convincing, as it was put forward on the basis of origin from them of the similar pretecto-rotundal inhibitory pathway that runs beginning from GABAergic neurons in these nuclei [7, 8, 70–73]. However, in mammals it is difficult to identify a pathway that is equivalent to the pretecto-rotundal pathway in reptiles and birds. This is due to that the mammalian neuronssources of GABAergic projections to LP-Pulv (a presumed homologue of n. rotundus in reptiles and birds) are located in the same pretectal nuclei (NOT, NOL, NPP, and NPA), in which pretecto-geniculate inhibitory connections also originate, although from other cell populations [74, 75]. The immunohistochemical


684

KENIGFEST et al.

characteristics of Ptv and Sub/IPS studied in our study and other works do not add any arguments in favor of identification of the single source of the pretectumLP-Pulv-pathway in mammals. In reptiles, Ptv is the nucleus with the most scanty and even lacking 5-HTIR, TH-IR, and SP-IR, whereas in mammals this is not the case, at any rate for NOT and NOL (see above). Among other pretectal nuclei participating in formation of the above pretecto-thalamic pathway, NPP and NPM contain Enk-IR cells, and, besides, NPP also has NPY-IR neurons, and all of them receive a scarce Enk and NPY innervation [31, 46]. As to Ptd, the issue of its homology with any mammalian nucleus is even less clear. In birds, it most probably corresponds to Pt that, like Ptd in reptiles, has GABAand NPY-IR neurons projecting to tectum [70, 76, 77]. In reptiles, Ptd receives a massive input from tectum [6, 8], but its function in both reptiles and birds [17] still remains obscure. Like Ptd in turtles, it practically lacks TH- and SP-IR projections and is poorly innervated with NPY-IR fibers. The most characteristic feature common to Ptd of reptiles and Pt of birds is a very high density (the highest in the turtle brain) of 5-HT innervation (our data, [25, 27, 41– 44]). The 5-HT terminal area in mammals, which has a comparable density, has been described in various retinorecipient and non-retinorecipient pretectal nuclei [38]. Thus, homology of Ptd in reptiles and Pt in birds might be suggested, but their homology with any particular pretectal nucleus in mammals remains unclear. ndCP (reptiles)–SPL (birds)–nCP (mammals). Two deepest non-retinorecipient nuclei, ndCP and Po, are combined in reptiles and birds by many authors to the single nucleus ndCP. This nucleus in the majority of reptiles and the corresponding SPL in birds represent a chain of the pallido-pretecto-tectal pathway of motor/visuomotor control. Their most characteristic feature is a high amount of Enk- and GABA-IR neurons projecting to ndCP and further to tectum [9–11, 26, 47, 78]. Although in mammals there has been described nCP connected with posterior commissure and projecting to CS [79, 80], it has no Enk-IR neurons [45, 46] and does not receive projections from pallidum (see [10, 78]), unlike that in reptiles and birds. Based on these data, a conclusion has been made that in mammals, unlike most reptiles and birds, the pallido-pretecto-tectal motor pathway that had existed in their reptilian ancestors was lost during evo-

lution or has remained as an extremely poorly developed structure, whereas the direct pallido-tectal pathway got an intensive development [9–11, 78]. In turtles, ndCP also contains NPY-IR and a very small amount of TH-IR cells that have not been previously described in turtles and other reptile species [26, 27, 57–60, 65]. The latter cells, also few in number, have been revealed in SPL of birds [56], but not in nCP of mammals. Thus, there are all reasons to believe that neurochemical characteristics of homologous nuclei of the pretectal posterior commissure might vary in amniotic brain evolution. Our previous study [8] has presented hodological and morphological data supporting identification of ndCP and Po as two independent nuclei. They have both similar and different sensory afferent connections [5, 81, 82]. The immunohistochemical characteristics of Po and ndCP revealed in the present work confirms, despite the similarity of innervation and the presence of Enk-, NPY-, and GABA-IR neurons in both nuclei, confirm the possibility of their divergence; however, it was impossible to find the Po-equivalent nucleus in birds and mammals. Thus, a comparative analysis of our own and literature data obtained on reptiles, birds, and mammals combined with results of hodological studies has shown that some nuclei of the pretectum (Lm and NOT, Pd/Apr and NOL, ndCP/SPL and nCP) and pathways running from them have a conservative organization in amniotes, but they have both similar and different neurochemical characteristics. Homology of other pretectal nuclei (Ptv and Sub/IPS), which can be traced in reptiles and birds, have not been found in mammals. Finally, left beyond the framework of discussion are several pretectal nuclei in mammals, for which it has not been yet possible to find equivalents in reptiles and birds. Probably, parcellation of pretectum in the course of evolution of various lines of amniotes has resulted in that their homologous cell populations are distributed in different, as a whole nonhomologous nuclei. This suggestion is based on the Nauta–Karten hypothesis for amniotic telencephalon [83, 84] and confirmed by Reiner for pretectal nuclei [18]. By the example of pretectum, it has been shown that neurochemical, as well as hodological, characteristics of brain structures and their projection pathways have a sufficiently high level of plasticity in evolutionary development, which leads both to acquisi-



tion and to loss of several features. This conclusion that seems true and is defended by many specialists [20, 23, 27] nevertheless requires a great caution and more thorough additional studies, which is due to great variability in detection of immunoreactivity to the studied substances not only in different amniote species, but also in the same species in works of different authors. It hardly might be explained by merely species differences or special methodical peculiarities in different studies. To a significant degree, this can be due to effects of quite a few factors (age, sex, seasonal factor, functional state of the animal, etc.) on various stages of synthesis and transport of biologically active substances, first of all of those that perform a modulator function, particularly neuropeptides and monoamines. It can be hoped that combination of comparative immunohistochemistry, hodology, and the currently proposed neuromeric embryogenetic approach [20, 63] will help solving many controversial issues of brain organization in reptiles and the further brain evolution in higher amniotes.

7.

8.

9.

10.

11.

12.

ACKNOWLEDGMENTS The work is supported by the Russian Foundation for Basic Research (projects nos. 99-04-49848 and 001597935).

13.

REFERENCES 14. 1.

2. 3.

4.

5.

6.

Butler, A.B. and Hodos, W., Comparative Vertebrate Anatomy. Evolution and Adaptation, New York: Wiley Liss, 1996. Senn, D.G., Notes on the Amphibian and Reptilian Thalamus, Acta Anat., 1974, vol. 87, pp. 556–596. Hergueta, S., Lemire, M., Ward, R., Rio, J.-P., and Repérant, J., A Reconsideration of the Primary Visual System of the Turtle Emys orbicularis, J. Hirnforsch., 1992, vol. 33, pp. 515–544. Repérant, J., Rio, J.-P., Ward, S., Hergueta, S., Miceli, D., and Lemire, M., Comparative Analysis of the Primary Visual System of Reptiles, Biology of the Reptilia, vol. 17, Neurology C, Chicago: Univ. Chicago, 1992, pp. 175–240. Reiner, A., Zhang, D., and Eldred, W.D., Use of Sensitive Anterograde Tracer Cholera Toxin Fragment B Reveals New Details of the Central Retinal Projections in Turtles, Brain Behav. Evol., 1996, vol. 48, pp. 307–337. Ulinski, P.S., Dacey, D.M., and Sereno, M.J., Optic Tectum, Biology of the Reptilia, vol. 17, Neurology C,

15.

16.

17.

18.

19.

685

Chicago: Univ. Chicago, 1992, pp. 241–366. Belekhova, M.G., Kenigfest, N.B., Vesselkin, N.P., Rio, J.-P., and Repérant, J., External Sources of GABAergic Innervation of Visual Centers of the Turtle Dorsal Thalamus, Dokl. Ross. Akad. Nauk, 1999, vol. 368, pp. 412–415. Kenigfest, N.B., Belekhova, M.G., Repérant, J., Rio, J.-P., Vesselkin, N.P., and Ward, R., Pretectal Connections in Turtles with Special Reference to the Visual Thalamic Centers: A Hodological and λ-Aminobutyric Acid Immunohistochemical Study, J. Comp. Neurol., 2000, vol. 426, pp. 31–50. Reiner, A., Brauth, S.E., Kitt, C.A., and Karten, H.J., Basal Ganglionic Pathways to the Tectum: Studies in Reptiles, J. Comp. Neurol., 1980, vol. 193, pp. 565– 589. Reiner, A., Medina, L., and Veenman, C.L., Structural and Functional Evolution of the Basal Ganglia in Vertebrates, Brain Res. Rev., 1988, vol. 28, pp. 235– 285. Medina, L. and Smeets, W.J.A.J., Comparative Aspects of the Basal Ganglia-Tectal Pathways in Reptiles, J. Comp. Neurol., 1991, vol. 308, pp. 614–629. Korf, H.-W. and Wagner, U., Nervous Connections of the Parietal Eye in Adult Lacerta sicula Rafinesque as Demonstrated by Anterograde and Retrograde Transport Horseradish Peroxydase, Cell Tiss. Res., 1981, vol. 219, pp. 567–583. Martinez-Marcos, A., Font, C., Lanuza, E., and Martinez-Garcia, F., Ascending Projections from the Optic Tectum in the Lizard Podarcis hispanica, Vis. Res., 1998, vol. 15, pp. 459–475. Belekhova, M.G. and Kenigfest, N.B., Pretectal and Tectal Connections of the Turtle Intergeniculate Foliaceous Nucleus Revealed by a Tracer Method, Zh. Evol. Biokhim. Fiziol., 2001, vol. 37, pp. 136–143. Fite, K.V., Pretectal and Accessory Optic Visual Nuclei of Fish, Amphibia and Reptiles: Theme and Variations, Brain Behav. Evol., 1985, vol. 26, pp. 71–90. McKenna, O.C. and Wulliman, J., Accessory Optic System and Pretectum of Birds: Comparison with Those of Other Vertebrates, Brain Behav. Evol., 1985, vol. 26, pp. 91–116. Gamlin, P.D.R. and Cohen, D.H., Projections of the Retinorecipient Pretectal Nuclei in the Pigeon (Columba livia), J. Comp. Neurol., 1988, vol. 269, pp. 18– 46. Reiner, A., Laminar Distribution of the Cells of Origin of Ascending and Descending Tectofugal Pathways in Turtles, Brain Behav. Evol., 1994, vol. 43, pp. 254– 292. Nieuwenhuys, H.J., Ten Donkelaar, H.J., and Nicolson, C., The Central Nervous System of Vertebrates, Berlin: Springer, 1998, pp. 1315–1524.


686

KENIGFEST et al.

20. Smeets, W.J.A.J. and González, A., Catecholamine Systems in the Brain of Vertebrates: New Perspectives through a Comparative Approach, Brain Res. Rev., 2000, vol. 33, pp. 358–379. 21. Parent, A., Comparative Anatomy of the Serotoninergic Systems, J. Physiol. (Paris), 1980, vol. 77, pp. 147–156. 22. Parent, A., Poitras, D., and Dubé, L., Comparative Anatomy of Central Monoaminergic Systems, Handbook of Chemical Neuroanatomy, vol. 2, part 1, Amsterdam: Elsevier, 1984, pp. 409–439. 23. Smeets, W.J.A.J. and Reiner, A., Catecholamines in the CNS of Vertebrates: Current Concepts of Evolution and Functional Significance, Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates, Cambridge: Cambridge Univ., 1994, pp. 463– 481. 24. Dávila, J.C., Guirado, S., and Puelles, L., Expression of Calcium-Binding Proteins in the Diencephalon of the Lizard Psamodromus algirus, J. Comp. Neurol., 2000, vol. 427, pp. 67–92. 25. Smeets, W.J.A.J. and Steinbusch, H.W.H., Distribution of Serotonin Immunoreactivity in the Forebrain and Midbrain of the Lizard Gekko gecko, J. Comp. Neurol., vol. 271, pp. 419–434. 26. Reiner, A., Neuropeptides in the Nervous System, Biology of the Reptilia, vol. 17, Neurology C, Chicago: Chicago Univ., 1992, pp. 587–739. 27. Smeets, W.J.A.J., Catecholamine Systems in the CNS of Reptiles: Structure and Functional Correlations, Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates, Cambridge: Cambridge Univ., 1994, pp. 103–133. 28. Curwen, A.O. and Miller, R.N., The Pretectal Region of the Turtle, Pseudemys scripta troostii, J. Comp. Neurol., 1939, vol. 71, pp. 99–120. 29. Belekhova, M.G., Kenigfest, N.B., Vesselkin, N.P., Repérant, J., and Rio, J.-P., Neuropeptide Y-Immunoreactivity in the Turtle Diencephalon and Midbrain, Zhurn. Evol. Biokhim. Fiziol., 1999, vol. 35, pp. 411– 421. 30. Belekhova, M.G., Kratskin, I.L., Repérant, J., Pierre, J., Vesselkin, N.P., Kenigfest, N.B., Tumanova, N.L., Chkheidze, D.D., Localization of GABA-Immunoreactive Elements in Thalamus of the Turtle Emys orbicularis, Zh. Evol. Biokhim. Fiziol., 1991, vol. 27, pp. 676–685. 31. Morin, L.P. and Blanchard, J.H., Neuropeptide Y and Enkephalin Immunoreactivity in Retinorecipient Nuclei in the Hamster Pretectum and Thalamus, Vis. Neurosci., 1997, vol. 14, pp. 765–777. 32. Morin, L.P. and Meyer-Bernstein, E.L., The Ascending Serotoninergic System in the Hamster: Comparison with Projections of the Dorsal and Median Raphe

Nuclei, Neuroscience, 1999, vol. 91, pp. 81–105. 33. Borostyanski, Z.A., Gorcs, T.J., and Hamori, J., Immunocytochemical Mapping of NPY and VIP Neuronal Elements in the Cat Subcortical Visual Nuclei with Special Reference to the Pretectum and Accessory Optic System, Anat. Embryol., 1999, vol. 200, pp. 495–508. 34. Simpson, J.I., Giolli, R.A., and Blanks, R.H.I., The Pretectal Nuclear Complex and the Accessory Optic System, Neuroanatomy of the Oculomotor System, Amsterdam: Elsevier, 1988, pp. 335–364. 35. Reiner, A., Krause, J.E., Keyser, K.T., Eldred, W.D., and McKelry, J.F., The Distribution of Substance P in Turtle Nervous System: A Radioimmunoassay and Immunohistochemical Study, J. Comp. Neurol., 1984, vol. 226, pp. 50–75. 36. Miguel-Hidalgo, J.J., Senba, E., Takatsuji, K., and Tohyama, M., Effect of Eye Enucleated on Substance P Immunoreactive Fibers of Some Retinorecipient Nuclei of the Rat in Relation to Their Origin from the Superior Colliculus, Neuroscience, 1991, vol. 44, pp. 235–241. 37. Medina, L. and Smeets, W.J.A.J., Cholinergic, Monoaminergic and Peptidergic Innervation of the Primary Visual Centers in the Brain of the Lizard Gekko gecko and Gallotia galotti, Brain Behav. Evol., 1992, vol. 40, pp. 157–181. 38. Steinbusch, H.W.H., Serotonin-Immunoreactive Neurons and Their Projections in the CNS, Handbook of Chemical Neuroanatomy, vol. 3, part 2, Amsterdam: Elsevier, 1984, pp. 68–125. 39. Jacobs, B.L. and Azmitia, E.C., Structure and Function of the Brain Serotonin System, Physiol. Rev., 1992, vol. 72, pp. 165–229. 40. Ueda, S., Takeuchi, Y., and Sano, Y., Immunohistochemical Demonstration of Serotonin Neurons in the Central Nervous System of the Turtle Clemmys japonica, Anat. Embryol., 1983, vol. 108, pp. 1–19. 41. Pierre, J., Repérant, J., Belekhova, M., Nemova, L., Vesselkin, N., and Miceli, D., Analyse Immunohistochemique du Système Sérotoninergique dans l’Encèphale du lézard Opisaurus apodus, C.R. Acad. Sci. Sér. III, 1990, vol. 311, pp. 43–49. 42. Bennis, M., Gamrani, H., Geffard, M., Calas, A., and Kah, O., The Distribution of 5-HT-Immunoreactive Systems in the Brain of a Saurian, the Chameleon, J. Hirnforsch., 1990, vol. 31, pp. 563–574. 43. Challet, E., Miceli, D., Pierre, J., Repérant, J., Masicotte, G., Herbin, M., and Vesselkin, N.P., Distribution of Serotonin Immunoreactivity in the Brain of the Pigeon (Columba livia), Anat. Embryol., 1996, vol. 193, pp. 209–227. 44. Challet, E., Pierre, J., Repérant, J., Ward, R., and Miceli, D., The Serotoninergic System of the Brain of



45.

46.

47.

48.

49.

50.

51. 52.

53.

54.

55.

56.

57.

58.

the Vipera aspis. An Immunohistochemical Study, J. Chem. Anat., 1991, vol. 4, pp. 233–248. Finley, J.C.W., Maderdrut, J.L., and Petrusz, P., The Immunocytochemical Localization of Enkephalin in the Central Nervous System of the Rat, J. Comp. Neurol., 1981, vol. 198, pp. 541–565. Fallon, J.H. and Leslie, F.M., Distribution of Dynorphin and Enkephalin Peptides in the Rat Brain, J. Comp. Neurol., 1986, vol. 249, pp. 293–336. Reiner, A., The Distribution of Proenkephalin-Derived Peptides in the Central Nervous System of Turtles, J. Comp. Neurol., 1987, vol. 259, pp. 65–91. Marchant, E.G. and Morin, L.P., The Hamster Circadian Rhythm System Includes Nuclei in the Subcortical Visual Shell, J. Neurosci., 1999, vol. 19, pp. 10 482–10 493. Distel, H. and Ebbesson, S.O.E., Habenular Projections in the Monitor Lizard (Varanus benegalensis), Exp. Brain Res., 1981, vol. 43, pp. 324–329. Mikkelsen, J.D. and Vrang, N., A Direct PretectoSuprachiasmatic Projection in the Rat, Neuroscience, 1994, vol. 62, pp. 497–505. Morin, L.P., The Circadian Visual System, Brain Res. Rev., 1994, vol. 19, pp. 102–128. Gregory, K.M., The Dendritic Architecture of the Visual Pretectal Nuclei of the Rat: A Study with the Golgi–Cox Method, J. Comp. Neurol., 1985, vol. 234, pp. 122–135. Klooster, J., Vrensen, G.F.J.M., Muller, L.J., and van der Want, J.J.L., Efferent Projections of the Olivary Pretectal Nucleus in the Albino Rat Subserving the Pupillary Light Reflex and Related Reflexes. A Light Microscopic Tracing Study, Brain Res., 1995, vol. 688, pp. 34–46. Björklund, A. and Lindvall, O., Dopamine-Containing Systems in the CNS, Handbook of Chemical Neuroanatomy, vol. 2, part 1, Amsterdam: Elsevier, 1984, pp. 55–122. Hökfelt, T., Martenson, R., Björklund, A., Kleinau, S., and Goldstein, M., Distribution of Tyrosine-Hydroxylase Immunoreactive Neurons in the Rat Brain, Handbook of Chemical Neuroanatomy, vol. 2, part 1, Amsterdam: Elsevier, 1984, pp. 277–379. Bailhache, T. and Balthazart, J., The Catecholaminergic System of the Quail Brain: Immunohistochemical Studies of Dopamine-Hydroxylase and Tyrosine Hydroxylase, J. Comp. Neurol., 1993, vol. 329, pp. 230–256. Smeets, W.J.A.J., Jonker, A.J., and Hoogland, P.V., The Distribution of Dopamine in the Forebrain and Midbrain of the Turtle (Pseudemys scripta elegans) Reinvestigated Using Antibodies against Dopamine, Brain Behav. Evol., 1987, vol. 30, pp. 121–142. Wolters, J.G., Ten Donkelaar, H.J., and Verhof-

59.

60.

61.

62.

63.

64.

65.

66.

67.

68.

69.

687

stad, A.J., Distribution of Catecholamines in the Brain Stem and Spinal Cord of the Lizard Varanus exanthematicus: An Immunohistochemical Study Based on Use of Antibodies to Tyrosine Hydroxylase, Neurosci., 1984, vol. 13, pp. 469–493. Smeets, W.J.A.J., Hoogland, P.V., and Voorn, P., The Distribution of Dopamine Immunoreactivity in the Forebrain and Midbrain of the Lizard Gekko gecko: An Immunohistochemical Study with Antibodies against Dopamine, J. Comp. Neurol., 1986, vol. 253, pp. 46–60. Smeets, W.J.A.J., Distribution of Dopamine Immunoreactivity in the Forebrain and Midbrain of the Snake Python regius: A Study with Antibodies against Dopamine, J. Comp. Neurol., 1988, vol. 271, pp. 115– 129. Reiner, A., Karle, E.J., Anderson, K.D., and Medina, L., Catecholaminergic Perykaria and Fibers in the Avian Nervous System, Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates, Cambridge: Cambridge Univ., 1994, pp. 135–181. Rodman, H.R. and Karten, H.J., Laminar Distribution and Sources of Catecholaminergic Input to the Optic Tectum of the Pigeon (Columba livia), J. Comp. Neurol., 1995, vol. 359, pp. 424–442. Puelles, L. and Verney, C., Early Neuromeric Distribution of Tyrosine Hydroxylase Immunoreactive Neurons in Human Embryos, J. Comp. Neurol., 1998, vol. 394, pp. 283–308. Medina, L., Marti, E., Artero, C., Fasolo, A., and Puelles, L., Distribution of Neuropeptide-Like Immunoreactivity in the Brain of the Lizard Gallotia galotti, J. Comp. Neurol., 1992, vol. 319, pp. 387–405. Bennis, M., Bamhamed, S., Rio, J.-P., Le Cren, D., Repérant, J., and Ward, R., The Distribution of NPYLike Immunoreactivity in the Chameleon Brain, Anat. Embryol., 2001, vol. 13, pp. 121–128. Aste, V.C., Viglietti-Panzica, C., Fasolo, A., Andreone, C., Vaudry, G.C., Pelletier, G., and Panzica, G.C., Localization of Neuropeptide Y (NPY) Immunoreactive Cells and Fibers in the Brain of Japanese Quail, Cell Tiss. Res., 1991, vol. 265, pp. 219–230. Naik, D.R., Sar, M., and Stumpf, W.E., Immunohistochemical Localization of Enkephalin in the Central Nervous System and Pituitary of the Lizard Anolis carolinensis, J. Comp. Neurol., 1981, vol. 198, pp. 583– 601. Bennis, M., Araneda, S., and Calas, A., Distribution of Substance P-Like Immunoreactivity in the Chameleon Brain, Brain Res. Bull., 1994, vol. 34, pp. 349– 357. Takasuji, K. and Tohyama, M., Differential Effect of Light on Substance P Immunoreactivity in Rat Suprachiasmatic and Olivary Pretectal Nucleus, Neu-


688

KENIGFEST et al.

roreport, 1993, vol. 6, pp. 647–650. 70. Granda, R. and Crossland, W.J., GABA-Like Immunoreactivity of Neurons in the Chicken Diencephalon and Mesencephalon, J. Comp. Neurol., 1989, vol. 287, pp. 455–469. 71. Ngo, T.D., Nemeth, A., and Tömböl, T., Some Data of GABAergic Innervation of Nucleus Rotundus in Chicks, J. Hirnforsch., 1992, vol. 33, pp. 335–355. 72. Mpodozis, J., Cox, K., Shimizu, T., Bischof, H.-J., Woodson, W., and Karten, H.J., GABAergic Inputs to the Nucleus Rotundus (Pulvinar Inferior) of the Pigeon (Columba livia), J. Comp. Neurol., 1996, vol. 374, pp. 204–222. 73. Deng, C. and Rogers, L.J., Organization of TectoRotundal and SP/IPS-Rotundal Projections in Chicks, J. Comp. Neurol., 1998, vol. 394, pp. 171–185. 74. Kubota, T., Morimoto, M., Kanaseki, T., and Inomata, H., Visual Pretectal Neurons Projecting to the Dorsal Lateral Geniculate Nucleus and Pulvinar Nucleus in the Cat, Brain Res. Bull., 1988, vol. 20, pp. 573–579. 75. Sudkampf, S. and Schmidt, M., Physiological Characterization of Pretectal Nucleus Projecting to the Lateral Posterior–Pulvinar Complex of the Cat, Eur. J. Neurosci., 1995, vol. 7, pp. 881–888. 76. Bagnoli, P., Fontanesi, G., Alesci, R., and Erichsen, J.T., Distribution of Neuropeptide Y, Substance P, and Choline Acetyltransferase in the Developing Visual System in the Pigeon, and Effects of Unilateral Retina Removal, J. Comp. Neurol., 1992, vol. 318, pp. 392– 414. 77. Gamlin, D.R., Reiner, A., Keyser, K.T., Brecha, N., and Karten, H.J., Projection of the Nucleus Pretec-

78.

79.

80.

81.

82.

83.

84.

talis to a Retinorecipient Tectal Layer in the Pigeon (Columba livia), J. Comp. Neurol., 1996, vol. 368, pp. 424–438. Medina, L. and Reiner, A., Neurotransmitter Organization and Connectivity of the Basal Ganglia in Vertebrates: Implications for Evolution of Basal Ganglia, Brain Behav. Evol., 1995, vol. 46, pp. 235–238. Kanaseki, T. and Sprague, J.M., Anatomical Organization of Pretectal Nuclei and Tectal Laminae in the Cat, J. Comp. Neurol., 1974, vol. 158, pp. 319–338. Taylor, A.M., Jeffery, G., and Lieberman, A.R., Subcortical Afferent and Efferent Connections of the Superior Colliculus in the Rat and Comparisons between Albino and Pigmented Strains, Exp. Brain Res., 1988, vol. 62, pp. 131–142. Künzle, H. and Woodson, W., Mesodiencephalic and Other Target Regions of Ascending Spinal Projections in the Turtle Pseudemys scripta elegans, J. Comp. Neurol., 1982, vol. 212, pp. 349–364. Desfilis, E., Font, E., and Garcia-Verdugo, J.M., Trigeminal Projections to the Dorsal Thalamus in a Lacertid Lizard, Podarcis hispanica, Brain Behav. Evol., 1998, vol. 52, pp. 99–110. Nauta, W.J.H. and Karten, H.J., A General Profile of the Vertebrate Brain in the Sidelight on the Ancestry of the Cerebral Cortex, The Neurosciences: Second Study Program, New York: Rockefeller Univ., 1970, pp. 7–26. Shimizu, T. and Karten, H.J., Central Visual Pathways in Reptiles and Birds: Evolution of the Visual System, Vision and Visual Disfunction, vol. 2, Evolution of the Eye and Visual System, Ann Arbor: CRC, 1991, pp. 421–441.
