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We have examined the subependymal region of the diencephalic third ventricle in notothenioid perciforms and report a pattern of neuropil expansions that appears to be phyletically derived for notothenioids and their outgroups but that is otherwise unique among vertebrates. We recognize five types of expansions based on their composition (from less dense neuropil to sacs) and width or protrusion into the third ventricle. In the species with the most elaborate morphology, Trematomus bernacchii, bilateral subependymal expansions fuse along the midline to form a single sac within the ventricular cavity. The extent of these expansions loosely corresponds with phyletic position but also (and perhaps more importantly) is correlated with the habitation of cold water (r2 = 0.48; P = 0.012). Furthermore, subependymal expansion type is positively correlated with the maximum size of the soma of neurons in two hypothalamic nuclei, the preopticus magnocellularis (r2 = 0.54; P = 0.006) and the lateralis tuberis (r2 = 0.40; P = 0.038). These nuclei project to the pituitary and contain cerebrospinal fluid-contacting neurons. In considering the functional consequences of this morphology, we cannot dismiss the possibility that these structures form a specialized enteroceptive system tied to the monitoring of cerebrospinal and extracellular fluid components, including antifreeze glycopeptides and inorganic ions.

Sprouted collateral axons were observed in the electrosensory lateral line lobe (ELL) of gymnotiform teleosts (Apteronotus leptorhynchus) following the ablation of the supraorbital branch of the anterior lateral line nerve. Ablation was accomplished by using microinjections of the toxic lectin ricin. Sprouted axons were followed for up to 26 weeks postablation. Ricin exposure severely reduced axonal numbers and the peripheral electroreceptors in the region innervated by these fibers. To visualize sprouted fibers, intact lateral line afferent nerve branches were anterogradely labelled with the neuronal tract tracers horseradish peroxidase or cobalt chloride, or the monoclonal antibody Q26A3. Within the four somatotopically organized ELL segments, sprouted collaterals were first observed two weeks after ricin injection in the medial and centromedial segments, and four weeks postinjection in the centrolateral and lateral segments. Sprouting involved intrasegmental, horizontally directed axons from adjacent nerve branch terminal fields, and mixed intra- and extrasegmental, dorsally directed axons from the ELL deep fiber layer. The sprouting response was robust but variable in its timing, peaking between 6 and 12 weeks. Subsequently, the intrasegmental, horizontally directed fibers were retained but the mixed dorsally directed fibers, including all extrasegmental axons, were retracted. Therefore, this sprouting response appears to consist of a collateral overproduction followed by a selective axonal retraction. In our view, the most likely explanation for this axonal retraction is that the descending inputs from the isthmus and the cerebellum, as well as commissural fibers from the contralateral ELL, maintain established somatotopic relationships by eliminating somatotopically mismatched sprouted collaterals.

Monoclonal antibody (mab) anti-zebrin II recognizes a single 36-kD polypeptide in Purkinje cells in the rat and fish cerebellum. In the adult rat, zebrin II+ Purkinje cells form, in each hemicerebellum, seven parasagittal bands interposed by zebrin II- bands. We show that, in rats, immunoreactivity first appears caudally at postnatal day 5 and spreads; all Purkinje cells are labelled by postnatal day 12. Subsequently, immunoreactivity is selectively lost so that by day 18 the adult pattern of zebrin II+/-immunoreactive bands is created. This pattern indicates two types of Purkinje cells according to developmental trajectory, zebrin II-/+/-. In the adult gymnotiform teleost Eigenmannia, Purkinje cells in the corpus cerebelli (CCb), lateral valvula cerebelli (VCbl), and eminentia granularis anterior (EGa) are zebrin II+. Purkinje cells in the eminentia granularis posterior (EGp) and medialis (EGm) and the medial valvula cerebelli (VCbm) are zebrin II-. Zebrin II antigenicity is first present at 6 days postspawning (P6) in the EGa and at P8 in the CCb. In the valvula, labelling does not appear until P29. Immunoreactivity in the CCb, VCBl, and the EGa persists in the adult, whereas in the VCbm Purkinje cells become zebrin II- before reaching adulthood. These developmental histories (zebrin II-/+ and zebrin II-/+/-) correspond to the patterns of Purkinje cell development in mammals. Additionally, Eigenmannia has a third class of Purkinje cells, in the EGp and EGm, that never express zebrin II immunoreactivity, indicating that zebrin II expression is not an obligatory feature of Purkinje cell development in all vertebrates.

We demonstrate that preterminal axons composing the primary afferent projection onto the four somatotopically organized electrosensory lateral line lobe (ELL) segments in weakly electric gymnotiform teleosts course in fundamentally different directions in the most commonly studied species. Afferents enter the deep fiber layer (dfl) of the ELL and course in variable, but species-specific, directions within a horizontal plane before turning dorsally to terminate within the deep neuropil layer of the ELL (dnl). Among the species considered here, apteronotids exhibit the tightest projection pattern. Afferents enter the rostral ELL from the anterior lateral line nerve ganglion (ALLNG) in a nonsomatotopic fashion. As they course horizontally, these fibers undergo a rostrocaudal somatotopic sorting along the ventrolateral border of the dfl, then turn within a horizontal plane to course medially across the ELL segments. These medially coursing horizontal fibers are sorted: they form sublaminae according to the nerve branch containing their peripheral axon. Horizontal axons then turn dorsally, form fascicles, and terminate within the dnl. Within the dorsal fascicles, axons run directly into the dnl with little deviation, and their terminal fields exhibit no appreciable spread. In sternopygids, dfl horizontal fibers course in directions orthogonal to those in apteronotids. Fibers enter the rostral ELL and course medially across segments before turning caudally within segments. Unlike apteronotids, sternopygid horizontal fibers do not sort tightly by nerve branch. As horizontal axons turn dorsally they also form tight fascicles. But rather than terminating directly and without spreading, as in apteronotids, sternopygid fibers disperse from these fascicles and become sorted horizontally a second time prior to terminating in the dnl.(ABSTRACT TRUNCATED AT 250 WORDS)

The somatotopically and functionally organized electrosensory system of gymnotiform teleosts provides a model for the study of the formation of ordered nerve connections. This paper describes the development of the major electrosensory nuclei within the hind- and midbrain. All three main electrosensory nuclei--the electrosensory lateral line lobe (ELL), dorsal torus semicircularis (torus), and tectum--grow by adding cells at their caudolateral borders. Toral and tectal germinal zones arise from lateral ventricular outpocketings that either completely or partially close by maturity. In the ELL before day 5 postspawning, germinal cells form from an initial periventricular germinal zone, then migrate to the caudolateral border of the hindbrain and begin dividing. The ELL grows from two main germinal zones, one for the medial segment, and one for the three lateral tuberous segments. Within each ELL germinal zone, newly formed cells arise from two areas: granular cells arise from a ventral subzone, pyramidal cells are generated more dorsally. Granular cells remain in situ, whereas pyramidal cells may migrate rostromedially. Cells begin differentiating as soon as they are formed. Spherical and pyramidal cells send ascending axons into the internal plexiform layer by day 14-18 and the ELL gradually begins to assume its mature laminar appearance. The ELL grows caudally, preceding the caudal lobe of the cerebellum, which will eventually lie over and fuse with it. Primary electrosensory afferents enter the ELL by day 6; incoming afferents form four fascicles within the ELL, suggesting the formation of separate ELL segments. Unlabelled projections between labelled fields from a single nerve branch filled with HRP on day 7 suggest that somatotopic order is already present at this early age. In the periphery, receptor addition is unordered, occurring along nerve branch pathways. Meanwhile the ELL adds cells in an orderly fashion at its caudolateral border. This suggests that primary afferents shift position caudally with growth to maintain their somatotopic relationships. Because all three central nuclei are in topographic register and grow by adding cells caudally, during growth ELL efferents to the torus and toral efferents to the tectum may utilize passive mechanisms, such as fiber-fiber interactions, to guide axons.

To determine the organizational principles underlying the peripheral electrosensory nervous system of weakly electric gymnotiform teleosts we labelled each of the four anterior lateral line nerve branches with HRP. We determined the position of labelled cell bodies within the ganglion and followed anterogradely filled fibers to their termination sites in one of the four somatotopic maps in the electroreceptive lateral line lobe (ELL). Within the ganglion, cell bodies exhibit a loose somatotopy based on nerve branch position: trunk electroreceptors have their cell bodies located in the caudal ganglion; cell bodies to the head receptors are rostral. Cell bodies to the head exhibit a rough dorsoventral polarity, supraorbital cells tend to be located dorsally, infraorbital cells centrally, and mandibular cells ventrally. Despite this general somatotopy there is substantial overlap (up to 30%) of cell bodies among regions. There appears to be no rostrocaudal topography within nerve branch regions. Iontophoretic WGA-HRP injected into the medial segment of the ELL retrogradely labelled cell bodies that innervate ampullary organs. These cell bodies were dispersed throughout the ganglion, indicating that cell bodies do not cluster by receptor type. Peripherally directed axons from the ganglion appear to undergo an active reorganization in order to form the nerve branches. Within nerve branches, axons to a particular area of skin do not cluster together. Centrally from the ganglion, axons retain the position of their cell body until they reach the ELL border. Once in the ELL, fibers become sorted in the deep fiber layer according to receptor type and the map they terminate in. This reorganization involves rearrangement of fascicles and axons within fascicles. In toto, proceeding from peripheral to central, the electrosensory periphery loses at least a portion of its receptor topography in the distal nerve and ganglion and then acquires both a functional and somatotopic organization after reaching the ELL; conceptually it is torn down and rebuilt again. From an ontogenetic perspective, axonal growth occurs from the ganglion outward; the fact that ganglion cell bodies are not highly organized while the receptors they innervate and their central processes are suggests that active axonal guidance mechanisms are involved.

The nerves of the anterior lateral line system in embryonic and larval stages of the weakly electric gymnotiform fish Eigenmannia were visualized by injection of the fluorescent marker DiI into the primordium of the anterior (ALLN) and posterior (PLLN) lateral line nerves. Examination of developmental series reveals that the nerve fibers that innervate the electrosensory and mechanosensory components of the anterior lateral line system are present before the first mechanoreceptors and electroreceptors have differentiated. This suggests that nerve fibers might induce the formation of lateral line receptors. Whereas the innervation of the mechanoreceptive system is already established at an early stage, the afferent innervation of electroreceptors continues to arborize in the periphery, presumably by following pioneer axon pathways. The earliest recognizable stage of the anterior lateral line nerve ganglion (ALLNG) is evident 2 days after spawning. The ganglion shows two germinal cell masses that develop into the supraorbital-infraorbital and the hyomandibular placodes. The supraorbital-infraorbital placode forms the dorsal part of the ALLNG; the hyomandibular placode forms the ventral part of the ALLNG. Counts of ALLNG cells in embryonic, larval, and adult stages of Eigenmannia show that, at each stage examined, the number of ganglion cells is always significantly larger than the number of mechanoreceptors and electroreceptor units in the periphery. During development, the distribution of ALLNG cell diameters shifts from a unimodal distribution in juveniles to a bimodal distribution in adults, peaking at 8 microns and 18 microns. These results suggest that tuberous electroreceptive organs, which are innervated by the large ALLNG cells, may not be functional prior to day 18. Our results further suggest that the number of ALLNG cells correlates with the rate of induction of lateral line receptors in the periphery.