Organization of retinal axons within the optic nerve, optic chiasm, and the innervation of multiple central nervous system targets Rana pipiens.

Light microscopic analysis of the optic nerve, chiasm, and optic tracts of Rana pipiens after the anterograde and retrograde transport of horseradish peroxidase has shown that retinal ganglion-cell axons reach the optic nerve head in chronotopically organized fascicles that form bands across the intraocular optic nerve. These bands of fascicles are divided along the midline in a "zone of reorganization" to create two full maps of the retinal surface; however, this map is discontinuous in that nasal and temporal quadrants are adjacent to one another. In the intracranial portion of the optic nerve, axons undergo another reorganization such that peripheral retinal axons shift position and become localized laterally and ventrally, whereas centrally placed axons become localized dorsally. Within this reorganization, the nerve is reconfigured into laminae of axons, and each lamina consists of age-related axons organized into two retinal maps. In the ipsilateral chiasm, axons diverge to form three central, optic tracts: the medial optic tract, the projection to the corpus geniculatum, and the basal optic root. Ipsilateral axons leave the chiasm at the same level of the chiasm as do their contralateral counterparts. The remaining axons converge in the lateral diencephalon to form a fourth fascicle, the marginal optic tract. Thus, within the optic chiasm, a sequence of positional transformations occur that result in the formation of multiple optic pathways. The various changes in axonal trajectory always coincide with changes in the orientation of cell groups that lie within the nerve and optic chiasm.

Single-unit responses to whole-field visual stimulation in the pretectum of Rana pipiens.

Visually responsive single units were recorded from the pretectal region that includes the large-celled nucleus lentiformis mesencephali (nLM) in the leopard frog, Rana pipiens. During monocular stimulation of the contralateral eye, 60 single units responding to movement of a large-field, random-dot pattern were quantitatively analyzed using horizontal and vertical directions at each of four pattern velocities (0.4-40 degrees/s). All units were spontaneously active, motion sensitive, and the majority showed 'on'-'off' responses. Several different response profiles were observed, including velocity-sensitive units with peak response at 10 degrees/s, most of which showed directional selectivity, and speed-sensitive units that showed increasing spike frequencies as pattern velocity increased, but little or no directional selectivity. About one-third of all unit analyzed were direction-selective, and 55% of those responded optimally to the temporal-to-nasal (T-N) direction of motion. T-N units were recorded primarily from an area that lies dorsolaterally between nLM and the optic tectum, in the 'peri-nLM' region. The pronounced monocular optokinetic nystagmus (OKN) response asymmetry that occurs in anurans appears to be reflected in the response profiles of the T-N direction selective units.

Segregation of optic axons based on central target: the medial optic tract in Rana pipiens.

The retinofugal projection to the nucleus of Bellonci (nB) was examined in Rana pipiens using both anterograde and retrograde transport of horseradish peroxidase (HRP). Following HRP injection into the nB, retrogradely labeled optic axons formed a discrete fascicle that crossed the lateral margin of the anterior diencephalon. We have designated this branch of the retinofugal pathway as the "medial optic tract." HRP-positive, medial optic tract axons projecting to nB occupied the rostral and most dorsal portion of the optic chiasm. The present findings indicate that within the optic chiasm, retinal axons are sorted according to their final destinations.

Organization of ascending projections from the optic tectum and mesencephalic pretectal gray in Rana pipiens.

The ascending projections from the dorsal mesencephalon to the thalamus and pretectum in Rana pipiens were investigated by using the anterograde and retrograde transport of HRP with regard to two major issues: (1) the degree of tectotopic organization in the projections, and (2) their cells of origin. The results indicate that the spatial organization of the tecto-thalamic tract is specifically related to the laminar organization of the contributing tectal efferent neurons. Axons of neurons in the superficial portion of tectal layer 8 exit the tectum through layer 9 and travel in the superficial portion of the dorsal and ventral tecto-thalamic tracts and innervate the nucleus lentiformis mesencephali, the posterior lateral dorsal nucleus, and corpus geniculatum. The distribution of terminals within these structures varied with the tectal HRP-injection site. HRP injections in the ventral tecto-thalamic tract retrogradely labeled neurons in the superficial portion of tectal layer 8 across the lateral and caudal portion of the tectal lobe. HRP injections into the dorsal tecto-thalamic tract, at the level of the pretectum, retrogradely labeled pyriform neurons in the superficial portion of tectal layer 8 in the rostral and medial portions of the tectal lobe. With regard to the deep tectal layers, axons from pyramidal neurons in layer 6 and ganglionic neurons in layer 8 leave the tectum through layer 7, travel in both the dorsal and ventral tecto-thalamic tracts, and are located internal to the axons of the pyriform neurons of superficial tectal layer 8. The majority of the ganglionic neurons project to the posterior lateral ventral nucleus and the anterior lateral nucleus. The distribution of terminals within these nuclei did not display a tectotopic organization. A second major projection to the thalamus originates from the mesencephalic pretectal gray and innervates the nucleus lentiformis mesencephali, the posterior lateral dorsal nucleus, the anterior lateral nucleus, dorsal and ventral divisions of the ventral lateral thalamus, and the nucleus of Bellonci. Other axons from the mesencephalic pretectal gray terminate in the contralateral, medial portions of the posterior lateral dorsal thalamus, the ventral lateral thalamus, and the anterior lateral nucleus. The isthmo-tectal projection was also retrogradely labeled following tectal injections of HRP. This pathway travels in the most ventral portion of the ventral tecto-thalamic tract; its axons passed over the lateral margin of the endopeduncular nucleus bilaterally, and crossed the midline in the caudal portion of the optic chiasm. Extensive, bead-like varicosities were observed on these axons both in the endopeduncular nucleus and in the posterior optic chiasm.(ABSTRACT TRUNCATED AT 400 WORDS)

Anatomical evidence for an intergeniculate leaflet in Rana pipiens.

The projections of the nucleus of Bellonci and the anterior thalamic nucleus in Rana pipiens appear to be remarkably similar to those that have been described for the mammalian intergeniculate leaflet. The connections of these nuclei were examined using both the anterograde and retrograde transport of horseradish peroxidase. Afferents to the neuropil of Bellonci and its nucleus include bilateral projections from the retina, the contralateral nucleus of Bellonci, and anterior thalamic nucleus as well as bilateral projections from the pretectum and the ipsilateral suprachiasmatic nucleus. Efferent projections observed following HRP injections in the anterior thalamus consist of three components: (1) a ventral hypothalamic-suprachiasmatic and commissural projection, (2) a dorsal descending tract to the pretectum and tectum, and (3) a ventral descending tract to the somatomotor brainstem.

Somatomotor connectivity in the midbrain of Rana pipiens.

The mesencephalic oculomotor nuclei of Rana pipiens and their surrounding cell groups were investigated using the anterograde and retrograde transport of horseradish peroxidase and Golgi techniques. The cell groups surrounding the oculomotor and trochlear nuclei were divided into the nucleus interstitialis (nInt) groups A, B, and C, the basal optic nucleus, and the nucleus reticularis tegmenti. Afferents to the ventral mesencephalon originate from the retina and from vestibular, cerebellar, visual, and accessory oculomotor nuclei. These afferents produce a sequence of terminal arborizations in which visual afferents are found in the outer neuropil, and accessory oculomotor, vestibular, and cerebellar afferents are found along the inner neuropil and central gray. The oculomotor neurons in anurans have extensive dendritic fields, extending to the outer margins of the neuropils, as do many large cells along the margin of nInt. Other neurons in nInt have dendritic fields restricted to the proximal portions of the neuropil. Efferents from nInt area A project to the cerebellum and bilaterally to the spinal cord. Area B nInt projects to the ipsilateral spinal cord, contralateral nInt, pretectal nucleus lentiformis mesencephali, and ipsilateral trochlear nucleus. Efferents from area C nInt reach the deep tectal layers and ipsilateral spinal cord. The outer portions of the neuropil contain the nucleus of the basal optic root which comprises ganglionic elongate and stellate neurons and projects to the pretectum. In the center of the neuropil peri-nBOR neurons have dendrites directed towards the visual terminal fields and axons towards the central gray and oculomotor neurons. The nucleus reticularis tegmenti receives afferents from the tectum and lateral forebrain bundle and projects to the deep tectal layers. In anurans, the oculomotor neurons receive a variety of visual, somatic, and vestibular afferents and appear relatively undifferentiated, whereas the nInt appears more developed.

Anuran accessory optic system: evidence for a dual organization.

The accessory optic system of Rana pipiens consists of lateral and medial fascicles of the basal optic root (BOR1, BORm) and a single terminal nucleus, nBOR. The present study provides new evidence that these two fascicles differ not only in their trajectories but in fiber spectra and innervation patterns as well. BOR1 contains a substantially higher percentage of large, myelinated axons than does BORm, and the mean diameter of axons in BOR1 is greater than that of BORm. BOR1 innervates the entire terminal field of nBOR, while BORm innervates only the central and mediodorsal portions of nBOR. The ventrolateral portion of nBOR is uniquely innervated by BOR1 and contains several types of neurons not found in the central and medial regions of nBOR which are innervated by both fascicles. Cytoarchitectural analysis of nBOR with Golgi techniques has revealed a number of similarities between the anuran nBOR and the mammalian medial terminal nucleus (MTN) with regard to cellular morphology, dendritic geometry, and retinofugal arborization patterns. In frog, nBOR appears comparable to the ventral subdivision of the mammalian MTN, while the peri-nBOR region, which contains neurons postsynaptic to nBOR, may represent a more primordial version of the mammalian dorsal MTN.

Projections of the vestibular and cerebellar nuclei in Rana pipiens.

The efferent projections and cytoarchitecture of the vestibulocerebellar region were examined to determine the nuclear boundaries and potential homologies. The anterior portion of the vestibular complex projects to the ipsilateral oculomotor and trochlear nuclei and is the major source of commissural fibers. Neurons in the rostromedial portions of the complex project to the contralateral trochlear nucleus. Large neurons in the ventrolateral portion of the complex give rise to a bilateral vestibulospinal pathway. Medium-sized neurons in the neuropil and small neurons in the central gray giving rise to bilateral projections to the spinal cord and oculomotor nuclei as well as commissural and ipsilateral cerebellar efferents. Projections from the nucleus of the cerebellum reach the contralateral spinal cord and cerebellar nucleus and there is also a bilateral projection to the ventral rhombencephalic and mesencephalic basal plates. The medial portion of the nucleus gives rise to commissural, ipsilateral mesencephalic and contralateral spinal projections. The lateral portion of the nucleus projects to the contralateral ventral mesencephalon. On the whole, the results of this investigation substantiate the division of the anuran vestibular complex in anurans into nuclei which may be homologous to the superior nucleus and nucleus of Deiters in mammals. The case for distinct descending and medial nuclei is less compelling. Further, it appears possible to divide the nucleus of the cerebellum into medial and lateral components whose connectivity is similar to that of reptiles and to a lesser extent mammals.

Thyrotropin-releasing hormone (TRH): immunohistochemical distribution in tadpole and frog brain.

The anatomical localization of immunoreactive TRH (IR-TRH) was demonstrated by the peroxidase-antiperoxidase technique in the brain and pituitary gland of larval and adult Rana catesbeiana. In the adult frog main sites of IR-TRH are perikarya and neuronal fibers in the preoptic and infundibular nuclei of the hypothalamus and in the amygdala and diagonal band of Broca of the telencephalon. In addition, TRH-positive neuronal fibers and endings were found in the septum, pallium, and brain stem as well as in the preoptico-hypophyseal tract, the external zone of the median eminence (which matures during late larval stages), and the pars nervosa; fibers were less extensive in the pars intermedia, and were absent from the pars distalis. In early larval stages, the magnocellular nucleus of the posterior preoptic area is the main site of immunoreactive perikarya. During late stages the extensive adult pattern of distribution of IR-TRH becomes established. The study represents the first immunohistochemical demonstration of IR-TRH in larval anurans, and serves as a basis for clarification of the neuroendocrine regulation of metamorphosis.

The pretectal nucleus lentiformis mesencephali of Rana pipiens.

The pretectal nucleus lentiformis mesencephali (nLM) of Rana pipiens was investigated with autoradiographic, horseradish peroxidase (HRP), and Golgi techniques. Retinal afferents to nLM originate primarily from the central retina. The primary projection is contralateral with a small ipsilateral component. Following optic nerve transection and HRP impregnation, contralateral retinal afferents show a restricted, dense core of HRP label in the superficial portion of the nucleus with sparser HRP label in the surround. Ipsilateral retinal afferents arborize throughout nLM, except in the dense-core region. Additional afferents to nLM originate from the ipsilateral tectum, the nucleus rotundus, the mesencephalic pretectal gray, the contralateral nLM, and the nucleus of the basal optic root. Afferents from the accessory optic system arborize only in the dense-core region, following HRP injections into the nucleus of the basal optic root, while afferents from the mesencephalic pretectal gray arborize in all parts of nLM except the dense core. Afferents from the tectum and anterior thalamus appear to arborize throughout the nucleus without discernible pattern. The lamination of afferent terminals in nLM was correlated with Nissl-stained cytoarchitectural material in which the majority of large neurons cluster around the dense core of nLM. Three types of neurons occur in nLM: large neurons (25-micron dia.), fusiform neurons (12.5-micron dia.), and stellate neurons (10-micron dia.). Additionally, two cell groups outside nLM which send dendrites into the nucleus were observed: cells of the posterior lateral nucleus and cells of the posterior thalamic pretectal gray. Both large and fusiform neurons project to the deep layers of the optic tectum as well as to the ventral rhombencephalon superficial to the abducens nucleus. While a small number of fusiform neurons project to the nucleus of the basal optic root, the stellate neurons appear to be intrinsic to nLM. The anuran nLM strongly resembles the nucleus of the optic tract in mammals in terms of the site of origin of its retinal afferents, lamination of afferent terminations, its central connections, and its demonstrated involvement in horizontal optokinetic nystagmus.