The organization of central auditory pathways in a reptile, Iguana iguana

The present experiments were designed to trace the central auditory pathways in an extant reptile, the New Worlkd lizard--Iguana iguana, utilizing anterograde axonal degeneration stained by the Fink-Heimer ('67) method and the retrograde axonal transport of horseradish peroxidase (LaVail and LaVail, '74). Beginning with the projections of the auditory portion of the VIIIth nerve, the ascending pathways were traced through successive relay nuclei to the telencephalon. The auditory portion of the VIIIth nerve projects to two nuclei in the dorsomedial medulla-nucleus angularis and nucleus magnocellularis medialis. These two nuclei together with a third cll group, nucleus magnocellularis lateralis (intercalated between nucleus angularis and nucleus magnocellularis medialis), have been referred to as the auditory tubercle in previous studies (cf. Miller, '75). The axonal degeneration following large lesions of the auditory tubercle and small lesions of nucleus angularis demonstrated the second order auditory pathways. Fibers leave nucleus angularis ventrally and travel to the ventral surface of the medulla where they cross the midline and ascend to the midbrain in pathways resembling the trapezoid body and the lateral lemniscus of mammals. Along these pathways, terminal arborizations of some fibers were seen in three lower brainstem nuclei while other fibers ascent to the midbrain and terminate in the central nucleus of the torus semicircularis. Experiments in which horseradish peroxidase injections were made in the torus semicircularis demonstrated that nucleus angularis is a primary source of second order auditory fibers to the midbrain and, in addition, that two of the lower brainstem targets of the auditory tubercle project to the torus semicircularis. These lower brainstem pathways were shown to be associated with the auditory system by electrophysiologically recording sound-evoked responses from clusters of cells in the torus semicircularis. Ascending fibers arising from the central nucleus of the torus semicircularis were followed rostrally where they entered the dorsal thalamus and terminated throughout nucleus medialis. Finally, a thalamotelencephalic auditory pathway was traced from nucleus medialis into the lateral forebrain bundle. Terminations of this pathway from nucleus medialis were seen in the medial dorsal ventricular ridge and in the striatum. It was concluded that the ascending auditory pathways of the iguana bear a remarkable resemblance to both the mammalian and avian auditory pathways from the level of the first order neurons in the VIIIth nerve to the level of the telencephalon. At the same time, there are important specializations of the auditory system in birds and mammals such as the development of particular lower brainstem nuclei. Nevertheless, a basic plan for the organization of the auditory system in terrestrial vertebrates can be recognized which invites comparisons with the vertebrate classes that remained in aquatic habitats...     

Modifications in the laminar organization of peptide-like immunoreactivity in the anuran optic tectum following retinal deafferentation

Substance P (SP)-, leucine-enkephalin (LENK)-, cholecystokinin octapeptide (CCK8)-, bombesin (BOM)-, and avian pancreatic polypeptide (APP)-like immunoreactivities were analyzed in the optic tectum of Rana pipiens 5-99 days after unilateral eye enucleation, or optic nerve ligation, by means of the peroxidase-antiperoxidase and indirect fluorescence single and double labeling methods. The normal pattern (Kuljis and Karten, '81, '82c) of peptide-like immunoreactivity was observed ipsilaterally to the operation. Contralateral deafferented tectae displayed conspicuous modifications in the normal pattern of peptide-like immunoreactivity unique to each of the substances studied. The modifications of peptide-like immunoreactivity observed varied depending both on the survival time and on the particular peptide analyzed, with either increment or diminution or disappearance--or combinations thereof--in the staining intensity of some of the peptide-positive bands in the superficial one-third (superficial neuropil) of the tectum. The onset of these changes is detectable immunocytochemically between the sixth and tenth day following deafferentation. By 2-4 weeks full expression of the long-term changes is reached with no apparent further modification up to the 99th postoperative day. The rapid onset of these phenomena suggests the existence of a previously unrecognized retinal ganglion cell terminal peptidergic contribution to the tectum and/or rapid transsynaptic effects. The former possibility is suggested by recent observations demonstrating peptide-like immunoreactivity for SP, LENK, CCK8 and BOM in the retinal stump of ligated optic nerves (Kuljis and Karten, '82b). The fact that no vertebrate retinal ganglion cells have been shown to contain any of these peptides (Brecha et al., '79; Famiglietti et al., '80; Eldred and Karten, '81; Karten et al., '82), however, argues against the possibility of a retinal terminal contribution to peptide-like immunoreactivity in the tectum and suggests that transsynaptic phenomena are involved.     

Fiber connections of the torus longitudinalis and optic tectum in holocentrid teleosts

Fiber connections of the torus longitudinalis (TL) and target(s) of toral recipient tectal neurons (pyramidal cells) in the optic tectum were examined by tract-tracing methods in holocentrids. Injections into the stratum marginale (SM) labeled neurons in the stratum opticum and stratum fibrosum et griseum superficiale (SFGS). They had superficial spiny dendrites, with a fan-shaped branching pattern in SM and a thick basal dendrite that gave rise to bushy horizontal branches at the boundary between the SFGS and the stratum griseum centrale (SGC), where an axon and a thin dendrite arose. The axon terminated in a middle cellular layer of the SGC, and the thin dendrite ramified slightly deeper to this cellular layer. The SM injections also labeled cells in the ipsilateral TL. Injections into either the lateral or the medial part of TL labeled terminals in the ipsilateral SM and neurons in the bilateral nucleus paracommissuralis (NPC) and nucleus subvalvularis and ipsilateral nucleus subeminentialis. Only medial TL injections labeled cells in the ipsilateral SGC. These neurons had a basal dendrite that branched in the middle cellular layer of SGC, suggesting that they receive inputs from the pyramidal cells and project back to the TL to form a closed circuit. Only lateral TL injections labeled terminals in the corpus cerebelli. A visual telencephalic portion projects to the NPC and sublayers of SGC, where dendrites of the pyramidal cells and SGC neurons ramify. The present results therefore suggest that the TL and SM are components of an intricate circuitry that exerts telencephalic descending visual influence on the optic tectum and corpus cerebelli.     

Synaptic organization of inhibitory circuits in the pigeon's optic tectum

The synaptic organization of inhibitory systems in the pigeon's optic tectum was studied with intracellular recording techniques. An extrapolation procedure based on response latency was used to determine the synaptic delay of the postsynaptic potentials (PSPs) and the velocity of conduction of the associated retinal axons. Tectal cells receive mostly disynaptic, trisynaptic or polysynaptic inhibition from retinal ganglion cells. However, evidence was found which together with previous studies raised the possibility of the existence of a direct inhibitory retino-tectal path. Our present results also suggest that inhibition is transmitted from the retina to the tectal cells by way of both, feedforward and feedback pathways.     

Laminar organization of peptide-like immunoreactivity in the anuran optic tectum

Peptide, 5-hydroxytryptamine (5-HT)-, tyrosine hydroxylase (TOH)-, and glial fibrillary acidic protein (GFAP)-like immunoreactivity was studied in the optic tectum of Rana pipiens. Peroxidase-antiperoxidase and indirect immunofluorescence single- and double-labeling methods were used to compare differential laminar distribution of each of these substances. Substance P (SP), leucine-enkephalin (LENK), cholecystokinin octapeptide (CCK8), bombesin (BOM), avian pancreatic polypeptide (APP), and possibly neurotensin display unique individual patterns of laminar distribution of processes and cell bodies throughout the tectum. A correlative analysis of the topographical distribution of SP, LENK, BOM, and APP on the basis of double-labeled sections shows a precise laminar segregation of these substances. Vasoactive intestinal peptide-, beta-endorphin-, and ranatensinlike immunoreactivity is consistently absent from our material. 5HT- and TOH-like immunoreactivity discloses a reticular array of fibers without clear evidence of laminar organization. This peptide-like laminar organization is particularly elaborate throughout the superficial neuropil of the optic tectum, the major retinorecipient zone. The pattern of lamination demonstrated in the present study differs in several important features from that previously described on the basis of several histological methods. The cells of origin of processes (axons and/or dendrites) in the superficial tectal neuropil may be either intrinsic or extrinsic to the tectum. Special reference is made to conflicting evidence regarding the possibility of a retinal contribution to peptide-like tectal lamination.     

Afferent connections of the optic tectum in lampreys: an experimental study

Tectal afferents were studied in adult lampreys of three species (Ichthyomyzon unicuspis, Lampetra fluviatilis, and Petromyzon marinus) following unilateral BDA injections into the optic tectum (OT). In the secondary prosencephalon, neurons projecting to the OT were observed in the pallium, the subhipoccampal lobe, the striatum, the preoptic area and the hypothalamus. Following tectal injections, backfilled diencephalic cells were found bilaterally in: prethalamic eminence, ventral geniculate nucleus, periventricular prethalamic nucleus, periventricular pretectal nucleus, precommissural nucleus, magnocellular and parvocellular nuclei of the posterior commissure and pretectal nucleus; and ipsilaterally in: nucleus of Bellonci, periventricular thalamic nucleus, nucleus of the tuberculum posterior, and the subpretectal tegmentum, as well as in the pineal organ. At midbrain levels, retrogradely labeled cells were seen in the ipsilateral torus semicircularis, the contralateral OT, and bilaterally in the mesencephalic reticular formation and inside the limits of the retinopetal nuclei. In the hindbrain, tectal projecting cells were also bilaterally labeled in the dorsal and lateral isthmic nuclei, the octavolateral area, the sensory nucleus of the descending trigeminal tract, the dorsal column nucleus and the reticular formation. The rostral spinal cord also exhibited a few labeled cells. These results demonstrate a complex pattern of connections in the lamprey OT, most of which have been reported in other vertebrates. Hence, the lamprey OT receives a large number of nonvisual afferents from all major brain areas, and so is involved in information processing from different somatic sensory modalities.     

Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.)

The afferent and efferent connections of the tectum opticum in the carp (Cyprinus carpio L.) were studied with the HRP method. Following iontophoretic peroxidase injections in several parts of the tectum anterograde transport of the enzyme revealed tectal projections to the lateral geniculate nucleus, dorsal tegmentum, pretectal nuclei, nucleus rotundus, torus longitudinalis, torus semicircularis, nucleus isthmi, contralateral tectum and to the mesencephalic and bulbar reticular formations.Tectal afferents were demonstrated by retrograde HRP transport in the area dorsalis pars centralis of the telencephalon, torus longitudinalis, torus semicircularis, nucleus isthmi, nucleus profundus mesencephali, several pretectal nuclei, dorsomedial and dorsolateral thalamic nuclei, nucleus of the posterior commissure, mesencephalic and bulbar reticular nuclei and nucleus ruber. Visuo-cerebellar circuitry was investigated by means of peroxidase injections in the various parts of the cerebellum. These experiments revealed indirect retino- and tecto-cerebellar pathways via the pretectal nuclei and the nucleus isthmi.     

Intraocular colchicine inhibits competition between resident and foreign optic axons for functional connections in the doubly innervated goldfish optic tectum

After unilateral optic tectum ablation in the goldfish, regenerating optic axons grow into the optic layers of the remaining ipsilateral tectal lobe and regain visual function. The terminal arbors of the foreign fibers are initially diffusely distributed among the resident optic axons, but within two months the axon terminals from each retina are seen to segregate into irregular ocular dominance patches. Visual recovery is delayed until after segregation. This suggests that the foreign fibers compete with the residents for tectal targets and that the segregation of axon terminations is an anatomical characteristic of the process. Here we investigate whether inhibiting axonal transport in the resident fibers inhibits competition with foreign fibers. The eye contralateral to the intact tectal lobe received a single injection of 0.1 μg colchicine, which does not block vision with the intact eye. We measured visual function using a classical conditioning technique. Segregation of axon terminations was examined shortly following visual recovery by autoradiography. The no-drug control fish showed reappearance of vision with the experimental eye at 9 weeks postoperatively and ocular dominance patches were well developed. Colchicine administered to the intact eye (resident fibers) several weeks postsurgery decreased the time to reappearance of vision with the experimental eye by several weeks. Autoradiography revealed some signs of axonal segregation but the labeled foreign axons were mainly continuously distributed. Administration of colchicine at the time of tectum ablation, or of lumicolchicine at two weeks postoperatively produced normal visual recovery times. Fast axonal transport of³H-labeled protein was inhibited by 1.0 and 0.5 μg but not by 0.1 μg of colchicine or by 1.0 μg of lumicolchicine. Previous studies showed that while 0.1 μg of colchicine does not block vision it is sufficient to inhibit axonal regeneration following optic nerve crush. We conclude that two retinas can functionally innervate one tectum without forming conspicuous ocular dominance columns, and that the ability of residents to compete with the in-growing foreign axons is very sensitive to inhibition of axoplasmic transport or other processes that are inhibited by intraocular colchicine.     

Development of output connections from the inferior colliculus to the optic tectum in barn owls

We studied the development of the projection from the external nucleus of the inferior colliculus (ICX) to the optic tectum (OT) in the barn owl. The projection was labeled by tracer application in vitro to either the OT or the ICX, or by staining ICX cells intracellularly with biocytin. The axons of ICX neurons bifurcated into an ascending branch that projected toward the OT and a descending branch that coursed caudally to an unknown target in the brainstem. Axons of the ICX were observed to grow into the OT from embryonic day 16 (E16) on. From E22 on, side branches of the axonal projections could be found within the OT. At the day of hatching (E32), the projection displayed a dorsoventral topography comparable to the adult owl; however, atopically projecting cells remained. The complexity of the axonal arborization in the adult barn owl was found to be slightly increased compared with the hatchling. The terminal area of individual ICX cells in the OT of the adult barn owl was still broad, a finding that had not been expected from the sharply defined physiological response properties of the bimodal neurons in the space map of the OT. However, the width of the termination zone was in accordance with the large dendritic tree of the adult ICX cells, because both spanned comparable angles in their respective maps. Our data suggest that a coarse projection from the ICX to the OT can develop without coherent sensory input and may, therefore, be innately determined.     

Morphology and laminar distribution of electrophysiologically identified cells in the pigeon's optic tectum: an intracellular study

The responses of 65 cells to electrical stimulation of the contralateral optic nerve were intracellularly recorded in the pigeon optic tectum by using micropipettes filled with a solution of horseradish peroxidase. Nineteen of them were successfully labeled. Microscopic examination of the filled cells shows that our sample includes six pyramidal, ten ganglion, two stellate, and one bipolar horizontal cells. Thus, pyramidal and ganglion neurons constitute the most numerous types of cells in our sample. Pyramidal cells were located in layer II but mostly in its non-retinorecipient part, and they had restricted ascending dendritic trees oriented orthogonal to the tectal lamination. Ganglion cells were located in layer III with one exception, which was in sublayer IIi. These cells had non-oriented dendritic trees which ramify over considerable distances. Terminal dendritic branches from a number of pyramidal and ganglion cells extended superficially well within the region of optic fibers termination. In our study, ganglion cells constituted the efferent tectal elements. Pyramidal cells responded to optic nerve stimulation with a pure EPSP, with an EPSP-IPSP sequence, or with a pure IPSP. Ganglion cells always exhibited an IPSP either alone or preceded by an EPSP. Stellate and bipolar cells responded with a pure EPSP. The study of the laminar distribution of labeled and non-labeled cells shows from surface to depth, a gradual increase in the number of cells responding with an EPSP-IPSP or with a pure IPSP and a gradual decrease in the number of those exhibiting a pure EPSP. The analysis of the sensitivity of EPSPs and IPSPs to high frequency optic nerve stimulation shows that monosynaptic as well as polysynaptic EPSPs can be recorded from cells in the non-retinorecipient tectal region, a number of ganglion and pyramidal cells receive a direct retinal excitatory input as their dendrites pass through the region of optic endings, most IPSPs are polysynaptic, some cells located in the retinorecipient region may receive direct retinal inhibitory connections.     

The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). I. Cytoarchitecture and connections

The posterior neocortex in the gray squirrel, Sciurus carolinensis, includes an extensive region which receives projections from the pulvinar. Previous studies have demonstrated that this cortical region can be subdivided on the basis of differences in cytoarchitecture and electrophysiologically defined representations of the visual field. The main purpose of the present paper was to determine whether these cortical subdivisions could be related to corresponding subdivisions in the pulvinar. The methods used to trace connections included anterograde degeneration, anterograde axonal transport of tritiated amino acids and the retrograde axonal transport of horseradish peroxidase. The results indicate that the pulvinar in this species contains at least three main subdivisions which can be distinguished by their cytoarchitecture and their patterns of connections. A caudal subdivision contains large, evenly-spaced neurons and receives bilateral input from the superficial, retinal-recipient layers of the superior colliculus. This caudal subdivision has reciprocal interconnections with a cytorchitectonically ditinct area in the temporal cortex. A rostro-lateral subdivision contains smaller, more lightly stained neurons which tend to form cluster. This subdivision receives only ipsilateral tectal input and projects to occipital area 18. This subdivision does not receive input form areas 17, 18, and 19, or form the temporal cortex. Finally, a rostro-medial subdivision is cytoarchitectonically similar to the rostro-lateral subdivision but receives little, if any, input form the superior colliculus. This rostro-medial area does, however, receive corticofugal projections form occipital areas 17, 18, and 19, and projects to area 19. These patterns of connections suggest that each of these subdivisions has close associations with the visual system. The question of whether similar subdivisions are present in the visual thalamus of other species is discussed.     

Quantitative histological studies of the optic tectum in six species of Notropis and Cyprinella (Cyprinidae, Teleostei).

Significant differences in stratification and size of the visual layers of the optic tectum were found between three clear-water minnows (Notropis amabilis, N. boops, Cyprinella venustas) and three turbid-water minnows (N. atherinoides, N. bairdi, and C. lutrensis). Correlations among a variety of neural structures suggested the importance of stratum marginale (SM), stratum opticum (SO), and stratum fibrosum et griseum superficiale (SFGS), stratum griseum centrale (SGC) and stratum periventriculare (SPV) in vision, of stratum album centrale (SAC) and SGC for olfaction, and of SPV for the processing of acoustico-lateral information.     

Neuronal organization of the optic tectum in the river lamprey, Lampetra japonica: a Golgi study.

The neuronal and laminar organization of the optic tectum (OT) in the river lamprey was studied using the rapid Golgi method. Based primarily on the distribution pattern of the dendrites, the OT neurons were divided into vertical, horizontal and stellate neurons. The river lamprey OT shows a laminar structure consisting of eight concentric strata. The stratum ependymale consists of several rows of ependymal cells. The stratum cellulare periventriculare contains one to two rows of vertical neurons. The stratum fibrosum periventriculare is thin and contains a few vertical neurons. The stratum cellulare et fibrosum internum consists of several alternating cellular and fibrous layers: a large variety of vertical and horizontal neurons are distributed in this stratum. The stratum fibrosum centrale consists of compact horizontal fiber bundles, among which a few horizontal neurons are disseminated. In the stratum cellulare et fibrosum externum, numerous fibers run horizontally in a loosely organized plexus; various types of vertical, horizontal and stellate neurons are distributed among these fibers. The stratum opticum is the main terminal area of the optic nerve, and contains stellate and horizontal neurons. The stratum marginale is a thin layer and consists of sparse populations of vertical and horizontal neurons. Besides the above outer to inner laminar structure, the OT is divided into medial (m-OT) and lateral parts (1-OT), based primarily on the distribution pattern of the dendrites. The dendrites of neurons in the m-OT are distributed almost exclusively within the OT. On the other hand, the dendrites of some neurons in the 1-OT extended into the confines of the torus semicircularis (TS), and conversely, the dendrites of some neurons in the TS are distributed in the 1-OT. These findings are discussed in relation to the neuronal and laminar organization of the OT in other lamprey species and to recent hodological studies.     

The motor nucleus of the facial nerve in the opossum (Didelphis marsupialis virginiana). Its organization and connections

The organization of the facial nucleus was studied in the opossum by localizing neurons which stin poorly for acetylcholinesterase activity following transection of identified facial rami. The caudal auricular representation is limited to the ventromedial extreme of the nucleus, whereas the neurons contributing to the cervical ramus are situated dorsally and medially. The zygomatic representation extends throughout the intermediate portion of the nucleus, apparently overlapping with that of the palpebral and rostral auricular muscles which is limited to the ventral extreme of the intermediate zone. The buccolabial area is particularly large in the opossum and encompasses most of the lateral facial enlargement. Midbrain-facial projections were identified from the superior colliculus, the midbrain tegmentum (particularly caudal ventromedial areas) and the red nucleus. The location of terminal degeneration in the facial nucleus following lesions within each of these areas was plotted and interpreted in light of facial organization. Of particular note is the fact that the fibers of rubral origin distribute preferentially to the zygomatic and, to some extent, buccolabial areas, whereas the ventromedial tegmental system distributes most strongly to the areas of caudal auricular, cervical, palpebral and rostral auricualar representation. The medial and intermediate regions of the facial nucleus receive a denser midbrain projection than does the lateral (buccolabial) area. In contrast, evidence was obtained for an extensive facial projection from the parvocellular reticular formation and the caudal spinal trigeminal nucleus which strongly favors the buccolabial enlargement. The possibility exists that the medial pontine and medullary reticular formation as well as portions of the dorsal column nuclei also have a facial projection. Spino-facial fibers arise rostral to the cervical enlargement and show a predilection for the medial facial enlargement (cervical and caudal auricular areas). Although some systems distribute preferentially to specific areas of the facial nucleus, overlap is present suggesting considerable integration.     

The sensory component of the facial nerve of a reptile (Lacerta viridis).

The sensory fibers of the facial nerve in Lacerta viridis have been studied with a silver impregnation method to follow the course of axonal degeneration. Destruction of the geniculate ganglion demonstrated the degenerated sensory component of the facial nerve adjacent to the anterior vestibular root. Within the lateral vestibular area the facial sensory fibers consist of numerous rootlets separated by vestibular fibers and cells. These rootlets may join to form a main or paired sensory tract that passes through the vestibular nuclei to enter the tractus solitarius and divide into a small ascending prefacial component and a major descending prevagal division. A few fibers continue into the postvagal part of tractus solitarius and extend caudally to terminate in the nucleus commissura infima. Prefacial fibers terminate along the periventricular gray while prevagal fibers terminate within the tractus solitarius on the dendrites of cells of nucleus tractus solitarius and near the periphery of the dorsal motor nucleus of X. There was no noticeable degeneration in the descendens tractus trigemini. Terminal degeneration to descendens nucleus trigemini and motor nucleus of VII followed the tractus solitarius course. Most facial sensory fibers are probably related to taste and other visceral information.     

The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). I. Cytoarchitectonic organization

The cytoarchitectonic organization of the posterior hypothalamus of the cynomolgus monkey (Macaca fascicularis) was analyzed in Nissl, Golgi, acetylcholinesterase, and reduced silver preparations. The region consists of a number of cell masses that differ considerably in their discreteness and in the homogeneity of their neuronal populations. The nuclei identified include: the medial mamillary nucleus (in which at least three distinct subdivisions can be recognized—a pars medialis, a pars lateralis, and a pars basalis); the small-celled nucleus intercalatus; the large-celled lateral mamillary nucleus; a single premamillary nucleus; the tuberomamillary nucleus; the posterior hypothalamic nucleus; the caudal extension of the lateral hypothalamic area; the supramamillary area; and the paramamillary nucleus (which appears to correspond to the nucleus of the nucleus of the ansa lenticularis of other workers). As a basis for the subsequent experimental study of the efferent connections of the posterior hypothalamus, the location of each of these cell masses is described and illustrated in a series of low-power photomicrographs, as are the form and distribution of the resident neuronal populations of the various components of themamillary complex as seen in Golgi preparations.