Development and organization of the lamprey telencephalon with special reference to the GABAergic system

Abstract

Lampreys, together with hagfishes, represent the sister group of gnathostome vertebrates. There is an increasing interest for comparing the forebrain organization observed in lampreys and gnathostomes to shed light on vertebrate brain evolution. Within the prosencephalon, there is now a general agreement on the major subdivisions of the lamprey diencephalon; however, the organization of the telencephalon, and particularly its pallial subdivisions, is still a matter of controversy. In this study, recent progress on the development and organization of the lamprey telencephalon is reviewed, with particular emphasis on the GABA immunoreactive cell populations trying to understand their putative origin. First, we describe some early general cytoarchitectonic events by searching the classical literature as well as our collection of embryonic and prolarval series of hematoxylin-stained sections. Then, we comment on the cell proliferation activity throughout the larval period, followed by a detailed description of the early events on the development of the telencephalic GABAergic system. In this context, lampreys apparently do not possess the same molecularly distinct subdivisions of the gnathostome basal telencephalon because of the absence of a Nkx2.1-expressing domain in the developing subpallium; a fact that has been related to the absence of a medial ganglionic eminence as well as of its derived nucleus in gnathostomes, the pallidum. Therefore, these data raise interesting questions such as whether or not a different mechanism to specify telencephalic GABAergic neurons exists in lampreys or what are their migration pathways. Finally, we summarize the organization of the adult lamprey telencephalon by analyzing the main proposed conceptions, including the available data on the expression pattern of some developmental regulatory genes which are of importance for building its adult shape.

Keywords: agnathans; cell proliferation; cyclostomes; evolution; olfactory bulbs; pallium; preoptic region; subpallium.

Figure 1

Midsagittal schematic drawings (A,C) and hematoxylin-stained sections (B,D) of different developmental stages of P. marinus illustrating the identifiable structures at the midline as well as the variations on the cephalic flexure and the shifting from ventral to dorsal of the olfactory placode and the nasal opening. (A) 4 mm embryo, (B) 18 dpf prolarvae, (C) 7,8 mm prolarvae, (D) 29 dpf prolarvae. (A,C) are reproduced from Sterzi (1907). Rostral is to the right. ds, dorsal sac; HB, hindbrain; hc, habenular commissure; i, infundibulum; llp, lower lip; lt, lamina terminalis; m, mouth; MB, midbrain; nh, neurohypophysis; nhd, nasohypophyseal duct; no, nasal opening; nt, notochord; op, olfactory placode; opm, oropharyngeal membrane; P, pineal organ; pc, posterior commissure; ph, pharynx; poc, postoptic commissure; por, postoptic recess; pr, preoptic recess; pt, posterior tuberculum; r, neuroporic recess; ulp, upper lip.

Figure 2

Horizontal (A,D), transverse (B,C,F), and sagittal (E) hematoxylin-stained sections of different developmental stages of P. marinus. (A) Early formation of the optic vesicles by bilateral evagination of the rostral neural tube in a 12-dpf embryo. (B) Section through the habenula, pineal gland, and the olfactory placode of a 14-dpf prolarvae. (C) Section of a 26-dpf prolarvae at the level of the habenular commissure dorsally and the postoptic commissure ventrally. Note the trajectory of numerous axons emerging from the telencephalic hemispheres (primordium of the stria medullaris) coursing to the contralateral side through the habenular commissure. (D) Section illustrating the growing telencephalic hemispheres with the projecting axons grouping in its caudodorsal portion (asterisks). (E) Sagittal section of a 26-dpf prolarvae showing the midline prosencephalic structures. (F) Section through the telencephalon of a late prolarvae showing at both sides the incipient anlage of the interventricular foramen (arrows). In (A,D,E) rostral is to the right. ds, dorsal sac; H, habenula; hc, habenular commissure; i, infundibulum; lt, lamina terminalis; MB, midbrain; nh, neurohypophysis; nhd, nasohypophyseal duct; no, nasal opening; nt, notochord; os, optic stalk; ov, optic vesicle; op, olfactory placode; P, pineal organ; pc, posterior commissure; poc, postoptic commissure; por, postoptic recess; pr, preoptic recess; pt, posterior tuberculum; sia, sulcus intraencephalicus anterioris; sip, sulcus intraencephalicus posterioris; T, telencephalon. Scale bars: (A,C,F) = 20 μm, (D) = 30 μm, (B,E) = 40 μm.

Figure 3

Cell proliferation in transverse sections of the developing sea lamprey forebrain after incubation of 4 (A,B,D,E), 16 (C,F), and 25 (G–I) days in BrdU. (A–C), and (G), as well as (D–F), and (I), illustrate comparable rostrocaudal levels in larvae of different size, whereas (H) is intermediate between (G) and (I). There is a general increase of immunolabeled cells with the increase of the BrdU exposure time. Note also that numerous migrating labeled cells are detected after 16 days of incubation with this marker (C,F), and that its number increases with longer incubations (25 days; G–I); most of them are located at dorsal (pallial) levels. In addition, a prominent BrdU labeling is present in the periventricular portion of the still small prethalamic eminence in all cases. Arrowheads point to laterally displaced labeled cells. OB, olfactory bulb; DM, dorsomedial neuropile; H, habenula; LP, lateral pallium; lt, lamina terminalis; MPO, medial preoptic nucleus; P, pineal organ; Pa, pallium; PE, prethalamic eminence; PEA, pallial extended amygdala; plv, posterior lateral ventricle; poc, postoptic commissure; PP, parapineal; pr, preoptic recess; RPa, rostral paraventricular area; S, striatum; SE, septum; SP, subpallium; VP, ventral pallium. Scale bars: (A,D,G) = 60 μm; (B,C,E,F,H,I) = 80 μm.

Figure 4

GABA-ir cells in the adult (A–C), developing prolarvae (D–I), and midlarval lamprey telencephalon (J). (A) Transverse section illustrating GABA-ir cells in the olfactory bulb, lateral and ventral pallium, pallial extended amygdala, striatum, and medial preoptic nucleus. (B) GABA-ir cells in the lateral pallium, and the pallial extended amygdala. (C) GABA-ir cells in the prethalamic eminence. Most of its GABA-ir cells are dispersed at intermediate levels, but a few can be observed at either the medial (ventricular; arrowhead) or lateral (superficial; arrow) borders. Transverse (D–G), and sagittal (H,I) sections of prolarvae of different size illustrating the early development of the telencephalic GABAergic cells. Note the increase in the number of GABA-ir cells as well as the progressive colonization of dorsal (pallial) areas. (J) GABA-ir cells in the olfactory bulb, septum, and median preoptic nucleus of a 50-mm larva. In sagittal sections (H,I), rostral is to the right. OB, olfactory bulb; DM, dorsomedial neuropile; f, fissura circularis; H, habenula; ic, interbulbar commissure; LP, lateral pallium; lt, lamina terminalis; MnPO, median preoptic nucleus; MPO, medial preoptic nucleus; nhd, nasohypophyseal duct; NMLF, nucleus of the medial longitudinal fascicle; nTPOC, nucleus of the tract of the postoptic commissure; op, olfactory placode; P, pineal organ; Pa, pallium; pc, posterior commissure; PE, prethalamic eminence; PEA, pallial extended amygdala; plv, posterior lateral ventricle; poc, postoptic commissure; PT, pretectum; PTh, prethalamus; RPa, rostral paraventricular area; S, striatum; SE, septum; SP, subpallium; SPV, subparaventricular area; Th, thalamus; TN, tuberal nucleus; VP, ventral pallium. Scale bars: (A) = 100 μm; (B) = 50 μm; (C) = 60 μm; (D–G,I) = 30 μm; (H) = 40 μm; (J) = 70 μm.

Figure 5

Midsagittal section of the prosencephalic roof plate in P. marinus illustrating the dorsal telencephalic/diencephalic limit in either the columnar or the segmental conceptions of the neural tube. 1, Edinger (1888); von Kupffer (1906); Heier (1948); Schöber (1964); Nieuwenhuys and Nicholson (1998); 2, Burckhardt (1894); 3, Sterzi (1907); Pombal and Puelles (1999); 4, Ahlborn (1883); Pombal et al. (2009); Martínez-de-la-Torre et al. (2011). ds, dorsal sac; hc, habenular commissure; ic, interbulbar commissure; ls, lamina supraneuroporica; It, lamina terminalis; mch, mesencephalic choroidal plexus; pc, posterior commissure; pir, pineal recess; vt, velum transversum.

Figure 6

Schematic drawings of a transverse section through the adult lamprey telencephalon and rostral hypothalamus showing the evolution of the nomenclature of the different nuclei and areas. BO, bulbus olfactorius; CS, corpus striatum; D, dorsal pallium; DM, dorsomedial telencephalic neuropile; Ld, lateral pallium, dorsal part; LP, lateral pallium; LSh; lobulus subhippocampalis; M, medial pallium; Lv, lateral pallium, ventral part; MPO, medial preoptic nucleus; nPr, nucleus preopticus; P, pineal organ; PA, preoptic area; PE, prethalamic eminence; PEA, pallial extended amygdala; Phip, primordium hippocampi; plv, posterior lateral ventricle; PMg, magnocellular preoptic nucleus; poc, postoptic commissure; por, postoptic recess; PP, parapineal; PPd, primordium pallium dorsalis; PPir, primordium piriforme; RPa, rostral paraventricular area; S, striatum; SHL, subhippocampal lobe; St, striatum; VP, ventral pallium; vt, impar telencephalic ventricle.