Intracellular and current source density analysis of pretectal input to the optic tectum of the frog

Objective

Electrophysiological examination of the ipsilateral pretectotectal projection has proved that pretectal cells elicit strong suppressive responses to the ipsilateral tectum. However, the neural mechanisms underlying the contralateral pretectotectal prejection are still obscure. The present study aimed to examine the synaptic nature of pretectal nuclei and contralateral tectal cells, and to demonstrate the spatiotemporal pattern of neuronal activity in the 2 main brain structures.

Methods

Intracellular recording and current source density (CSD) analysis were used to test the complexity of neuronal mechanism of pretectotectal information transfer.

Results

The pretectal stimulation elicited only one type of response on the contralateral tectum, the inhibitory postsynaptic potential (IPSP). The majority of contra-induced IPSPs were assumed to be polysynaptically driven. In the CSD analysis, only one sink with short latency was observed in each profile. The ipsilateral projection produced a prominent monosynaptic sink in layer 8 of tectum. Recipient neurons were located in layers 6 and 7 of tectum. The result confirmed former findings from ipsilateral intracellular recordings.

Conclusion

These results suggest the following neuronal circuit: afferents from the pretectal nuclei broadly inhibit both tectal neuron, and since no second sink occurs in tectal layers, the pretectotectal excitatory afferents probably do not extend over the whole tectum, but are within limited state. The results of intracellular recording and CSD analysis further provide evidence of how pretectal afferent activity flows within the tectal laminae.     

Retinal projection to the pretectal nucleus lentiformis mesencephali in pigeons (Columba livia)

In birds, the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali (LM) are retinal‐recipient nuclei involved in the analysis of optic flow and the generation of the optokinetic response. The nBOR receives retinal input from displaced ganglion cells (DGCs), which are found at the margin of the inner nuclear and inner plexiform layers, rather than the ganglion cell layer. The LM receives afferents from retinal ganglion cells, but whether DGCs also project to LM remains unclear. To resolve this issue, we made small injections of retrograde tracer into LM and examined horizontal sections through the retina. For comparison, we also had cases with injections in nBOR, the optic tectum, and the anterior dorsolateral thalamus (the equivalent to the mammalian lateral geniculate nucleus). From all LM injections both retinal ganglion cells and DGCs were labeled. The percentage of DGCs, as a proportion of all labeled cells, varied from 2–28%, and these were not different in morphology or size compared to those labeled from nBOR, in which the proportion of DGCs was much higher (84–93%). DGCs were also labeled after injections into the anterior dorsolateral thalamus. The proportion was small (2–3%), and these DGCs were smaller in size than those projecting to the nBOR and LM. No DGCs were labeled from an injection in the optic tectum. Based on an analysis of size, we suggest that different populations of retinal ganglion cells are involved in the projections to LM, nBOR, the optic tectum, and the anterior dorsolateral thalamus. J. Comp. Neurol. 522:3928–3942, 2014. © 2014 Wiley Periodicals, Inc.     

Parallel organization of the avian sensorimotor arcopallium: Tectofugal visual pathway in the pigeon (Columba livia)

The sensory–motor division of the avian arcopallium receives parallel inputs from primary and high-order pallial areas of sensory and vocal control pathways, and sends a prominent descending projection to ascending and premotor, subpallial stages of these pathways. While this organization is well established for the auditory and trigeminal systems, the arcopallial subdivision related to the tectofugal visual system and its descending projection to the optic tectum (TeO) has been less investigated. In this study, we charted the arcopallial area displaying tectofugal visual responses and by injecting neural tracers, we traced its connectional anatomy. We found visual motion-sensitive responses in a central region of the dorsal (AD) and intermediate (AI) arcopallium, in between previously described auditory and trigeminal zones. Blocking the ascending tectofugal sensory output, canceled these visual responses in the arcopallium, verifying their tectofugal origin. Injecting PHA-L into the visual, but not into the auditory AI, revealed a massive projection to tectal layer 13 and other tectal related areas, sparing auditory, and trigeminal ones. Conversely, CTB injections restricted to TeO retrogradely labeled neurons confined to the visual AI. These results show that the AI zone receiving tectofugal inputs sends top-down modulations specifically directed to tectal targets, just like the auditory and trigeminal AI zones project back to their respective subpallial sensory and premotor areas, as found by previous studies. Therefore, the arcopallium seems to be organized in a parallel fashion, such that in spite of expected cross-modal integration, the different sensory–motor loops run through separate subdivisions of this structure.     

GABAergic inputs to the nucleus rotundus (pulvinar inferior) of the pigeon (Columba livia)

The avian nucleus rotundus, a nucleus that appears to be homologous to the inferior/caudal pulvinar of mammals, is the major target of an ascending retino-tecto-thalamic pathway. Further clarification of the inputs to the rotundus and their functional properties will contribute to our understanding of the fundamental role of the ascending tectal inputs to the telencephalon in all vertebrates, including mammals. We found that the rotundus contains a massive plexus of glutamic acid decarboxylase (GAD)-immunoreactive axons using antibodies against GAD. The cells within the rotundus, however, were not immunoreactive for GAD. The retrograde tracer cholera toxin B fragment was injected into the rotundus to establish the location of the afferent neurons and determine the source of the gamma-aminobutyric acid (GABA) inputs into the rotundus. In addition to the recognized bilateral inputs from layer 13 of the tectum, we found intense retrograde labeling of neurons within the ipsilateral nuclei subpretectalis (SP), subpretectalis-caudalis (SPcd), interstitio-pretecto-subpretectalis (IPS), posteroventralis thalami (PV), and reticularis superior thalami (RS). All the neurons of the SP, SPcd, IPS, and PV were intensely GAD-immunoreactive. The neurons of layer 13 of the tectum were not immunoreactive for GAD. Following the destruction of the ipsilateral SP/IPS complex, we found a major reduction in the intensity of the GAD axonal immunoreactivity within the ipsilateral rotundus, but this destruction did not diminish the intensity of the GAD-immunoreactivity within the contralateral rotundus. Our studies indicated that the source of the massive GAD-immunoreactive plexus within the rotundus was from the ipsilateral SP, SPcd, IPS, and PV nuclei. These nuclei, in turn, received ipsilateral tectal input via collaterals of the neurons of layer 13 in the course of their projections upon the rotundus. We suggest that the direct bilateral tecto-rotundal projections are excitatory, whereas the indirect ipsilateral projections from the SP/IPS and PV are mainly inhibitory, possibly acting via a GABA-A receptor. © 1996 Wiley-Liss, Inc.     

Receptive field properties of single cells in the pigeon's optic tectum during cooling of the ‘visual wulst’

In birds, efferents from the visual telencephalon (visual wulst) terminate in the ipsilateral and contralateral optic tectum. This study concerns the influence of a bilateral cryogenic block of the wulst on the receptive field properties of the visual tectal cells in the pigeon. Tectal units were tested for their responses to static and moving stimuli before, during and after cooling the wulst. For some units the cryogenic block of the wulst was repeated twice. The responsiveness to static and moving stimuli was decreased in most of the tectal cells when the neural activity of the wulst was blocked. In contrast, in some units cooling the wulst provokes an increase of responsiveness. These results indicate that the wulst-tectum path is able to convey both excitatory and inhibitory influences.Other receptive field properties such as the spatial location of the light and dark excitatory regions in the field, the effect of the surround, the size and shape of the excitatory region, the relative responsiveness to static and moving stimuli and the ‘spontaneous activity’ were not affected by wulst cooling.Directional tuning curves were obtained in 18 directionally selective cells before, during and after wulst cooling. In 6 of them the cryogenic block provoked a reduction in directional selectivity either by way of a reduction of the preferred response (4 cells) or by way of an increase of the non-preferred responses (2 cells). In two others directionally selective cells, cooling the wulst provoked a total loss of directional selectivity due to a reduction of the response to the preferred direction together with an increase of the response to the null direction. These results show: (1) that the retinal directional selective input to the tectum is affected by the cryogenic block of the wulst; and (2) that the visual wulst provokes a sharpening of the directional tuning at the optic tectum level.     

Catecholaminergic subpopulation of retinal displaced ganglion cells projects to the accessory optic nucleus in the pigeon (Columba livia)

In birds, displaced ganglion cells (DGCs) constitute the exclusive source of retinal input to the nucleus of the basal optic root (nBOR) of the accessory optic system. Tyrosine-hydroxylase (TH) immunoreactivity was examined in the pigeon retina after injections of rhodamine-labeled microspheres into the nBOR. A population of about 400 DGCs was observed in each case to exhibit both TH immunoreactivity and rhodamine bead fluorescence. This corresponded to about 10-15% of the total number of identified DGCs in each retina. Double-labeled cells were medium- to large-size (12 to 20 microns in the largest axis) and were always located at the border between the inner nuclear and the inner plexiform layers. Their dendrites could be followed horizontally in lamina 1 of the inner plexiform layer for up to 300 microns from the cell body. The distribution of double-labeled DGCs appeared to be mostly peripheral, matching the overall distribution of identified DGCs. Larger DGCs (21-28 microns) were never seen to contain TH immunoreactivity. Examination of brain sections revealed plexuses of thin varicose TH-positive axons in all subdivisions of the nBOR. Unilateral enucleation produced an almost complete elimination of TH immunoreactivity in the contralateral nucleus. Such results suggest the existence of a population of catecholaminergic DGCs projecting into the accessory optic system of the pigeon. They also support the emerging hypothesis concerning the neurotransmitter heterogeneity of ganglion cells in the vertebrate retina.     

A second ascending visual pathway from the optic tectum to the telencephalon in the pigeon (Columba livia)

Previous studies in the pigeon (Karten and Revzin: Brain Res. 2:368-377, '66; Karten and Hodos: J. Comp. Neurol. 140:35-52, '70) have described an ascending tectofugal visual pathway from the optic tectum to the ectostriatum by way of the nucleus rotundus of the thalamus. This present study used anterograde autoradiographic and retrograde horseradish peroxidase pathway-tracing techniques to investigate another ascending tectofugal pathway in the pigeon. Injections of 3H-proline/leucine confirmed a previous report that the optic tectum projects to the nucleus dorsolateralis posterior of the thalamus (DLP). This projection is predominantly ipsilateral and is confined to a large-celled caudal region of the nucleus (DLPc); the rostral region of the nucleus (DLPr) is not tectorecipient. Injections of horseradish peroxidase in DLPc labeled cells predominantly ipsilaterally in layers 8-15 of the optic tectum. Injections of 3H-proline/leucine placed in the DLPc labeled a discrete region of the ipsilateral telencephalon. Similar injections of DLPr labeled a contiguous, but more rostral, region of the neostriatum intermedium. Nissl- and silver-stained material indicated that the region in which DLP terminates is cytoarchitecturally distinct from ventromedial ectostriatal core and belt. Injections of horseradish peroxidase at various locations in the neostriatal DLP terminal field demonstrated a rostrocaudal ordering of the DLP projection upon the neostriatum intermedium. Single-unit recording demonstrated that cells in DLPc respond to whole-field illumination at the same latency as cells in the nucleus rotundus, indicating that the tecto-DLPc-neostriatal pathway transmits visual information to the telencephalon. We suggest that comparable pathways may exist in both reptiles and mammals.     

Retinal removal up-regulates cannabinoid CB(1) receptors in the chick optic tectum

The endocannabinoid system has been implicated in several neurobiological processes, including neurodegeneration and neuroprotection. The aim of this study was to evaluate the effects of unilateral retinal ablation on the expression of the cannabinoid receptor subtype 1 (CB(1)) at both protein and mRNA levels in the optic tectum of the adult chick brain. After different survival times postlesion (2-30 days), the chick brains were subjected to immunohistochemical, immunoblotting, and real-time PCR procedures to evaluate CB(1) expression. TUNEL and Fluoro-Jade B were used to verify the possible occurrence of cell death, and immunostaining for the microtubule-associated protein MAP-2 was performed to verify possible dendritic remodeling after lesions. No cell death could be observed in the deafferented tectum, at least up to 30 days postlesion, although Fluoro-Jade B could reveal degenerating axons and terminals. Retinal ablation seems to generate an increase of CB(1) protein in the optic tectum and other retinorecipient visual areas, which paralleled an increase in MAP-2 staining. On the other hand, CB(1) mRNA levels were not changed after retinal ablation. Our results reveal that CB(1) expression in visual structures of the adult chick brain may be negatively regulated by the retinal innervation. The increase of CB(1) receptor expression observed after retinal removal indicates that these receptors are not presynaptic in retinal axons projecting to the tectum and suggests a role of the cannabinoid system in plasticity processes ensuing after lesions.     

Two distinct populations of tectal neurons have unique connections within the retinotectorotundal pathway of the pigeon (Columba livia)

The tectofugal pathway is a massive ascending polysynaptic pathway from the tectum to the thalamus and then to the telencephalon. In birds, the initial component of this pathway is known as the tectorotundal pathway; in mammals, it is known as the tectopulvinar pathway. The avian tectorotundal pathway is highly developed; thus, it provides a particularly appropriate model for exploring the fundamental properties of this system in all amniotes. To further define the connectivity of the tectorotundal projections of the tectofugal pathway, we injected cholera toxin B fragment into various rotundal divisions, the tectobulbar projection, and the ventral supraoptic decussation of the pigeon. We found intense bilateral retrograde labeling of neurons that stratified within layer 13 and, in certain cases, granular staining in layer 5b of the optic tectum. Based on these results, we propose that there are two distinct types of layer 13 neurons that project to the rotundus: 1) type I neurons, which are found in the outer sublamina of layer 13 (closer to layer 12) and which project to the anterior and centralis rotundal divisions, and 2) type II neurons, which are found in the inner sublamina of layer 13 (closer to layer 14) and which project to the posterior and triangularis rotundal divisions. Only the labeling of type I neurons produced the granular dendritic staining in layer 5b. An additional type of tectal neuron was also found that projected to the tectobulbar system. We then injected Phaseolus vulgaris-leucoagglutinin in the optic tract and found that the retinal axons terminating within tectal layer 5b formed narrow radial arbors (7–10 μm in diameter) that were confined to layer 5b. Based on these results, we propose that these axons are derived from a population of small retinal ganglion cells (4.5–6.0 μm in diameter) that terminate on the distal dendrites of type I neurons. This study strongly indicated the presence of a major bilateral oligosynaptic retinotectorotundal pathway arising from small retinal ganglion cells projecting to the rotundus with only a single intervening tectal neuron, the proposed type I neuron. We suggest that a similar organization of retinotectopulvinar connections exist in reptiles and in many mammals. J. Comp. Neurol. 387:449–465, 1997. © 1997 Wiley-Liss, Inc.     

Postsynaptic potentials in neurons of the pigeon''s optic tectum in response to afferent stimulation from the retina and other visual structures: an intracellular study

The responses of the cells in the pigeon's optic tectum to electrical stimulation of the contralateral optic nerve, the ipsilateral visual Wulst and the opposite optic tectum were intracellularly recorded. Optic nerve or visual Wulst stimulation elicited 3 types of responses: (1) a pure EPSP which gave rise to one or two action potentials; (2) an EPSP which sometimes gave rise to a spike, followed by an IPSP; and (3) a pure IPSP. Opposite tectum stimulation evoked in the tectal cells either a pure IPSP or a pure EPSP. The mono- or polysynaptic nature of the pathways involved in the excitatory and inhibitory responses of the tectal cells was assessed by increasing the frequency of the optic nerve stimulation. At low stimulus rates (2-6 Hz), all the excitatory events showing latencies longer than 5 ms were blocked suggesting that they were polysynaptic. Excitatory events having latencies shorter than 5 ms were generally able to follow high rate frequencies of optic nerve stimulation (40, 50 or 90 Hz) and we considered them to be monosynaptic. All but 3 IPSPs evoked by optic nerve stimulation, were blocked by stimulus rates beyond 5 Hz. Thus, although most IPSPs are generated through polysynaptic paths, direct retino-tectal inhibitory paths may also exist. The latency of the responses of individual cells to optic nerve, visual Wulst and opposite tectum stimulation show that the polysynaptic IPSPs to optic nerve stimulation did not involve relays in the visual Wulst or the opposite tectum.     

A banded distribution of retinal afferents within layer 9A of the normal frog optic tectum

A banded distribution of retinal ganglion cell axons within layer 9A of the superficial tectal neuropil in Rana pipiens was revealed through anterograde labeling with horseradish peroxidase. Layer 9A previously has been demonstrated to mediate binocular vision through a polysynaptic pathway by way of the nucleus isthmi^5,8,9. This nucleus interconnects analogous regions of the two tectal lobes such that isthmic axons retinotopically map the visual world of the ipsilateral eye within tectal layers 9A and 8^9,10. Thus, we have found that a pattern of retinal ganglion cell bands occurs in binocular regions of normal frogs. This pattern is similar, but not identical, to the experimentally produced stripes previously observed in the doubly innervated tecta of 3-eyed and single tecta frogs^2,12–14. Qualitative and quantitative comparisons of these two types of afferent segregation patterns have implicated several structural and functional parameters which might be involved in band formation.     

Laminar distribution and sources of catecholaminergic input to the optic tectum of the pigeon (Columba livia)

A combined immunohistochemical and retrograde tracing approach was used to characterize the catecholaminergic innervation of the optic tectum (TeO), the major target of retinal projections in many avian species. Giemsa counterstaining was employed to determine precisely the laminar localization of immunoreactive fibers and presumptive terminals. The TeO of the pigeon is densely innervated by fibers immunoreactive for tyrosine hydroxylase (TH), which are most heavily distributed to the superficial layers of its dorsal and anterior portions. Within the dorsal-anterior tectum, TH-immunoreactive processes are particularly dense in retinorecipient layers 4 and 7 and in layer 5a. As in the mammalian superior colliculus, the bulk of the catecholaminergic innervation of the pigeon TeO reflects inputs, presumably noradrenergic, originating in the locus coeruleus and nucleus subcoeruleus. However, the catecholaminergic innervation of the pigeon TeO shows several features distinct from those reported for the mammalian superior colliculus. These include an input from a pretectal TH-positive cell group unknown in mammals and the presence of residual TH immunoreactivity after administration of the noradrenergic neurotoxin DSP-4. Moreover, the pattern of TH-immunoreactive fibers in pigeon TeO, indicates more laminar and regional specialization within this structure than has been reported for the catecholaminergic innervation of the superior colliculus in mammals. © 1995 Wiley-Liss, Inc.     

Fine structure of the visual dorsolateral anterior thalamic nucleus of the pigeon (Columba livia): a hodological and GABA-immunocytochemical study

The ultrastructure of the lateroventral subcomponent of the visual dorsolateral anterior thalamic nucleus of the pigeon (DLLv) was analyzed using hodological techniques and GABA-immunocytochemistry. Two types of GABA-immunonegative hyperpalliopetal neurons and a single type of strongly GABA-immunoreactive (-ir) interneuron were identified, the latter displaying long dendrites with some containing synaptic vesicles (DCSV). Ten types of axon terminal were identified and divided into two categories. The first, GABA-immunonegative and making asymmetrical synaptic contact, contain round (RT1, RT2, RT3) or pleiomorphic synaptic and many dense-core vesicles (DCT). RT1 terminals are retinothalamic and RT2 terminals hyperpalliothalamic; both mainly contact dendrites of projection neurons (72% and 78% respectively), less frequently dendrites of interneurons and sometimes DCSV; RT1 terminals are rarely involved in synaptic triads. The second category are consistently GABA-immunopositive. Four types (PT1-4), distinguished by their pleiomorphic synaptic vesicles, make symmetrical synaptic contact essentially with dendrites of projection neurons, more rarely on dendrites of interneurons (PT2). PT1 terminals are very probably those of interneurons, whereas the rare PT4 terminals are of retinal origin. A fifth type (RgT) contains round synaptic vesicles and makes asymmetrical synaptic contact with dendrites of projection neurons and interneurons. PT2 and RgT terminals occasionally contact DCSV of interneurons, which are sometimes involved in synaptic triads. Two final subcategories (DCgT1-2) contain many dense-core vesicles. Our findings are compared with those of previous studies concerning the fine structure and neurochemical properties of the GLd of reptiles and mammals, with special reference to the origin of the extraretinal and extracortical projections to this structure.     

An ascending visual pathway to the dorsal telencephalon through the optic tectum and nucleus prethalamicus in the yellowfin goby Acanthogobius flavimanus (Temminck & Schlegel, 1845)

Dual visual pathways reaching the telencephalon appear to be an ancient vertebrate trait, but some teleost fish seem to possess only one pathway via the optic tectum. We undertook the present study to determine if and when this loss occurred during evolution. Tracer injection experiments to the optic nerve, the optic tectum, and the dorsal telencephalon were performed in the present study, to investigate ascending visual pathways to the dorsal telencephalon in an acanthopterygian teleost, the yellowfin goby Acanthogobius flavimanus (Temminck & Schlegel, 1845). We confirmed the presence of a nucleus prethalamicus (PTh) in the goby, which has been convincingly identified only in holocentrids, suggesting that this nucleus is present in other acanthopterygians. We found that the optic tectum projects to the PTh bilaterally. The PTh projects in turn to the dorsal telencephalon, ipsilaterally. These results suggest that the yellowfin goby possesses only an extrageniculate‐like pathway, while a geniculate‐like pathway could not be identified. This situation is common with that of holocentrids and may be a character common in acanthopterygians. It is possible that a geniculate‐like system was lost in the common ancestor of acanthopterygians, although the scenario for the evolution of ascending visual systems in actinopterygians remains uncertain due to the lack of precise knowledge in a number of actinopterygian taxons.     

Immunohistochemical analysis of the visual wulst of the pigeon (Columba livia)

The avian wulst, a laminated "bulge" in the dorsal telencephalon, contains several distinct regions. The posterolateral portion (visual wulst) has been proposed to be an avian equivalent of the mammalian striate cortex. The present study examines specific neurotransmitters and neuropeptides within the visual wulst by immunohistochemical techniques. Antisera and monoclonal antibodies against choline acetyltransferase (ChAT), nicotinic acetylcholine receptor (nAChR), tyrosine hydroxylase (TH), serotonin (5-HT), glutamic acid decarboxylase (GAD), gamma-aminobutyric acid A receptor (GABAAR), cholecystokinin (CCK), substance P (SP), leucine-enkephalin (L-ENK), neurotensin (NT), neuropeptide Y (NPY), somatostatin (SRIF), corticotropin-releasing factor (CRF), and vasoactive intestinal polypeptide (VIP) were used. Somata and neuropil displaying specific immunoreactivity were generally distributed in accordance with the laminar cytoarchitectonic organization of the wulst. The superficial layer of the wulst, the hyperstriatum accessorium, contained the highest densities of TH-, 5-HT-, SP-, NPY-, SRIF-, CRF-, and VIP-positive neuropil in the wulst, whereas the highest density of CCK- and NT-staining was found in the deepest layer of the wulst, the hyperstriatum dorsale. In addition to the traditionally defined four laminae of the wulst, the immunoreactive staining revealed several subregions within each lamina. The most dorsolateral portion of the wulst contained the highest densities of ChAT- and L-ENK-stained fibers in the wulst, as well as moderately dense staining of neuropil for 5-HT-, TH-, SP-, and CCK-like immunoreactivity. The nAChR-immunoreactivity was faint and distributed rather uniformly throughout the wulst. The results suggest that the wulst consists of multiple regional variations within layers comparable to laminar variations found within different cytoarchitectonic areas of the mammalian neocortex.     

Fine structure of the optic fiber termination layer in the tectum of the teleost Rutilus: a stereological and morphometric study

The stratum fibrosum et griseum superficiale (SFGS) of the Rutilus optic tectum, which receives a massive fiber projection from the contralateral retina, was studied by electron microscopy. The qualitative and quantitative analysis of the laterodorsal (LD) portion of the stratum involved both a stereological examination of the different elements and a morphometric study of the various profiles containing synaptic vesicles (PCSVs). The relative volume of each element in the LD SFGS was as follows: myelinated and unmyelinated axons, 6.6%; PCSVs, 38%; dendrites without vesicles, spines, and cell bodies, 41.7%; glia, 10.5%. With the fixation employed, 35% of PCSVs showed spheroidal synaptic vesicles. These profiles could be subdivided into three types: (1) S1 (23.5%) represented optic terminals, since they degenerated after retinal ablation or were labeled after intraocular injection of HRP or [3H] proline. Three subgroups of S1 were identified: S1m--profiles containing clear mitochondria;S1c--profiles that were contiguous with S1m and lacked mitochondria;S1i--isolated profiles without mitochondria. (2) S2 (9.3%) were characterized mainly by their dark mitochondria. (3) S3 (2.2%) corresponded to small nonvisual terminals that were isolated and lacked mitochondria. The PCSVs with pleiomorphic synaptic vesicles (65%) were subdivided into three groups: P1 (38%), P2 (19%), and P3 (8%). P1 and P2 were axonal in nature; P2 could be distinguished from P1 by a greater density of synaptic vesicles. P3 was of dendritic origin. Analysis of synaptic patterns revealed a small number of serial synapses. The presynaptic elements were optic boutons, whereas the intermediate profiles were dendrites with synaptic vesicles (P3). Results are compared with ultrastructural data obtained in the superficial tectal layers of other teleosts and other vertebrate groups.     

Distribution, laminar location, and morphology of tectal neurons projecting to the isthmo-optic nucleus and the nucleus isthmi, pars parvocellularis in the pigeon (Columba livia) and chick (Gallus domesticus): a retrograde labelling study.

Retrograde transport of Phaseolus vulgaris leucoagglutinin (PHA-L), fluorogold, fast blue, rhodamine labelled microspheres, and horseradish peroxidase (HRP) was employed to study the distribution, laminar location within the optic tectum, and morphology of tectal cells projecting upon the isthmo-optic nucleus (ION) and the nucleus isthmi, pars parvocellularis (Ipc), in the pigeon and chick. Following injections into the ION, all retrograde markers labelled tecto-ION neurons and their dendrites in the ipsilateral tectum. The cells were located within a relatively narrow band at the border between layers 9 and 10 of the stratum griseum et fibrosum superficiale (SGFS). Retrogradely labelled neuronal somata were different in both dendritic branching and shape; however, tecto-ION neurons generally possessed non-spiny radially oriented and multi-branched dendrites. The apical processes extended into the retino-recipient layers (2-7) of the SGFS and basal dendrites extended into layers 12-14 of the SGFS. Positive neuronal somata were observed throughout the rostro-caudal extent of the optic tectum. The average distance between adjacent tecto-ION neurons varied from one region to another. Specifically, retrogradely labelled cells were more numerous in the caudal, lateral, and ventral tectum, and less numerous at rostro-dorsal levels. Approximately 12,000 tecto-ION neurons were labelled within the ipsilateral optic tectum following either PHA-L or fluorescent dye injections. While the regional distribution of tecto-Ipc neurons was not examined, the morphology indicated that the cells had a single radially oriented dendritic process. Therefore, the apical dendrites are more restricted than those of tecto-ION cells. Moreover, the dendrites were spiny and arborized within layers 3, 5, and 9 of the ipsilateral optic tectum. The axon of tecto-Ipc cells arise from the apical process as a shepherd's crook and descend into the deep layers of the optic tectum. These results indicate that 1) tecto-ION and tecto-Ipc neurons are possibly monosynaptically activated by retinal input, 2) tecto-ION neurons are heterogeneous in morphology, and 3) there is a differential distribution of the tecto-ION neurons throughout the rostro-caudal extent of the optic tectum, suggesting a greater representation of the caudo-ventral portion of the optic tectum within the ION. The discussion primarily concerns the organization of the retino-tecto-ION-retinal circuit in light of the distribution and morphology of tecto-ION neurons within the optic tectum.     

The mapping of the visual field onto the dorso-lateral tectum of the pigeon (Columba livia) and its relations with retinal specializations

Most of the physiological studies of the pigeon retino-tectal visual pathway have investigated the accessible tectum, a small dorso-lateral tectal section that can be easily accessed by a simple craniotomy. However, at present we lack a detailed study of the topographical arrangement between the visual field, the retina and the accessible tectum. In particular, it is not known which section of the visual field is mapped onto the accessible tectum, and which of the specialized retinal areas mediates this projection. Here we determined, using local field potential (LFP) recordings and reverse retinoscopy, the shape, size and position in the visual space of the portion of the visual field mapped onto the accessible tectum (called here the accessible visual field, or AVF). Using this data and the mapping of Nalbach et al. [Vis. Res. 30 (4) (1990) 529], the retinal area corresponding to the AVF was determined. Such retinal area was also directly delimited by means of retrograde transport of DiI. The results indicate that the AVF is a triangular perifoveal zone encompassing only 15% of total visual field. The retinal region corresponding to the AVF has the shape of an elongated triangle that runs parallel to the visual equator and contains the fovea, the tip of the pecten, a perifoveal region of the yellow field and a small crescent of the red field. In agreement with this anatomical heterogeneity, visual evoked potentials measured in different parts of the accessible tectum present steep variations in shape and size. These results are helpful to better design and interpret anatomical and physiological experiments involving the pigeon's visual system.     

Projections of the nucleus of the basal optic root in pigeons (Columba livia) revealed with biotinylated dextran amine

The nucleus of the basal optic root (nBOR) of the accessory optic system is known to be involved in the analysis of the visual consequences of self-motion. Previous studies have shown that the nBOR in pigeons projects bilaterally to the vestibulocerebellum, the inferior olive, the interstitial nucleus of Cajal, and the oculomotor complex and projects unilaterally to the ipsilateral pretectal nucleus lentiformis mesencephali and the contralateral nBOR. By using the anterograde tracer biotinylated dextran amine, we confirmed these projections and found (previously unreported) projections to the nucleus Darkshewitsch, the nucleus ruber, the mesencephalic reticular formation, and the area ventralis of Tsai as well as ipsilateral projections to the central gray, the pontine nuclei, the cerebellar nuclei, the vestibular nuclei, the processus cerebellovestibularis, and the dorsolateral thalamus. In addition to previous studies, which showed a projection to the dorsomedial subdivision of the contralateral oculomotor complex, we found terminal labelling in the ventral and dorsolateral subdivisions. Individual fibers were reconstructed from serial sections, and collaterals to various nuclei were demonstrated. For example, collaterals of fibers projecting to the vestibulocerebellum terminated in the vestibular or cerebellar nuclei; collaterals of fibers to the inferior olive terminated in the pontine nuclei; many individual neurons projected to the interstitial nucleus of Cajal, the nucleus Darkshewitsch, and the central gray and also projected to the nucleus ruber and the mesencephalic reticular formation; collaterals of fibers to the contralateral nucleus of the basal optic root terminated in the mesencephalic reticular formation and/or the area ventralis of Tsai; neurons projecting to the nucleus lentiformis mesencephali also terminated in the dorsolateral thalamus. The consequences of these data for understanding the visual control of eye movements, neck movements, posture, locomotion, and visual perception are discussed. J. Comp. Neurol. 384:517–536, 1997. © 1997 Wiley-Liss, Inc.