Abnormal retinotopic organization of the dorsal lateral geniculate nucleus of the tyrosinase-negative albino cat

Visual defects associated with hypopigmentation have been studied extensively in Siamese and albino cats. Previous research on tyrosinase-negative albino cats has shown that (1) approximately 95% of all nasal and temporal retinal fibers cross at the optic chiasm, and (2) ocular dominance columns normally found in cortex are replaced with hemiretinal domains. In this study, we compared the retinotopic organization of the dorsal lateral geniculate nucleus (LGNd) and visual cortex in albino cats. Extracellular recordings were conducted in the LGNd, area 17, and area 18 of six albino cats. Receptive fields (RFs) were plotted for all sites. We find that, as in albino visual cortex, the albino LGNd contains (1) normal cells with RFs in the visual hemifield contralateral to the recording site (RFc), (2) abnormal cells with RFs in the ipsilateral hemifield (RFi), (3) abnormal cells with dual, mirror-symmetric RFs, one in each hemifield (RFd), and (4) abnormal cells with broad RFs that span the vertical meridian (RFb). Our data indicate that lamina A and lamina A1 consist predominantly of normal RFc and abnormal RFi cells, respectively. The C laminae contain a mixture of RFc, RFi, RFd, and RFb cells. The interlaminar zones contained RFd cells, RFb cells, or both. Thus, the albino LGNd is arranged into hemiretinal and not ocular dominance laminae. Finally, the percentage of normal cells is significantly larger in area 17 (84%) and area 18 (70%) than in the LGNd (46%), suggesting a suppression of abnormal activity in albino cat cortex, which could underlie the existing competence of visual function in albinos.     

Ventral lateral geniculate nucleus projects to the dorsal lateral geniculate nucleus in the cat

The lamina C3 of the dorsal lateral geniculate nucleus of the cat does not receive retinal projections but instead receives visual information from the small subpopulation of W-type ganglion cells via the upper substratum of the stratum griseum superficiale of the superior colliculus. We herein report a projection from the lateral division of the ventral lateral geniculate nucleus into the lamina C3 of the dorsal lateral geniculate nucleus. As the lateral division receives projections from the contralateral retina and the ipsilateral upper stratum griseum superficiale of the superior colliculus, we suggest that these regions make up a small cell type W-cell neuronal network that provides visual information to layer I of the striate cortex via the lamina C3.     

Neurons of the dorsal lateral geniculate nucleus of the albino rat.

Light and electron microscopic observations were made on the dorsal lateral geniculate nucleus (DLGN) of 33 young adult male albino rats. Three variants of the Golgi silver impregnation technique were employed in the light microscopic studies. Neurons were classified into three categories based on location, dendritic pattern, and dendritic appendages. Type 1 and type 3 neurons were distributed throughout the DLGN. Type 2 neurons were located in the superficial zone. Dendritic appendages of type 1 and type 2 neurons indicated these cells may function as geniculo-cortical relay neurons. The type 3 neurons had lobulated dendritic appendages and an axon that terminated withinthe nucleus. Type 3 neurons may represent Golgi-type-II interneurons. Camera lucida drawings, photomicrographs, and electronmicrographs illustrate the characteristics ofthe three cell types. The literature on ultrastructural and neurophysiological findings may substantiate the presence of three neuronal types. Initially, the rat DLGN does not appear as elaborately organized as the nucleus observed in cats and primates; however, there are notable similarities in neuronal morphology and synaptology.     

The projection of the lateral geniculate nucleus to area 18

The present study is concerned with the projection of the lateral geniculate nucleus onto cortical area 18. Horseradish peroxidase (HRP) was injected into area 18 of 15 cats. Drawings were made to determine the location of the injection site and the distribution of labeled neurons in the lateral geniculate nuclei of each cat. The local retinotopic maps constructed prior to the injections and the reconstructions of the lateral geniculate nucleus were used to determine the location and the extent of each of the HRP injections. In 15 of the 25 hemispheres studied, the ratio of the number of HRP-labeled neurons in lamina A relative to the number of labeled neurons in lamina A1 was calculated. This ratio varied from 1.06 to 0.28, indicating that at least some regions of area 18 are dominated by inputs from lamina A1. However, if the HRP-labeled neurons in lamina C are included in the counts for lamina A, then the ratio A + C/A1 has a mean of 1.11, suggesting that area 18 receives a balanced input, with inputs from the contralateral eye being relayed through laminae A and C, and inputs from the ipsilateral eye being relayed through lamina A1. When the distribution of HRP-labeled neurons in lamina A was plotted onto a dorsal view of the lateral geniculate nucleus, the labeled neurons formed an ellipse with the long axis of the ellipse oriented parallel to the isoelevation lines. The representation of azimuth is compressed in area 18 relative to the lateral geniculate nucleus. In six hemispheres the injections were restricted to a few layers of the area 18. Following small injections into layer IV of area 18, the HRP-labeled neurons occupied an extensive region of the lateral geniculate nucleus, indicating a considerable amount of convergence of the inputs to area 18. In hemispheres where the injections were restricted to layers I and II, labeled neurons were only seen in the medial interlaminar nucleus and the C laminae.     

Response properties of cells in the dorsal lateral geniculate nucleus of the albino rat

The response patterns of cells in the dorsal lateral geniculate nucleus of the albino rat were studied in order to examine the functional organization of the lateral geniculate nucleus. Both photic stimulation and electrical stimulation of the optic tract were used to activate single units in the lateral geniculate nuclei. Three different types of response patterns were found for principal cells, while interneurons all had similar response patterns. The first class of principal cells, E-S cells, responded to stimulation with a period of excitation, followed by a period when activity was suppressed. A second class of cells, S cells, responded to photic stimulation with an initial period when activity was suppressed. The final class of cells, E cells, responded with a period of excitation followed by a return to spontaneous rates of firing. The response patterns of E cells suggest that this type of principal neuron does not receive feedback inhibition of the type proposed in previous models of the lateral geniculate nuclei. Based on these and other observations, a new model of the functional organization of the lateral geniculate nuclei is proposed.     

Synaptic organization of thalamocortical axon collaterals in the perigeniculate nucleus and dorsal lateral geniculate nucleus

We examined the synaptic targets of large non-gamma-aminobutyric acid (GABA)-ergic profiles that contain round vesicles and dark mitochondria (RLD profiles) in the perigeniculate nucleus (PGN) and the dorsal lateral geniculate nucleus (dLGN). RLD profiles can provisionally be identified as the collaterals of thalamocortical axons, because their ultrastrucure is distinct from all other previously described dLGN inputs. We also found that RLD profiles are larger than cholinergic terminals and contain the type 2 vesicular glutamate transporter. RLD profiles are distributed throughout the PGN and are concentrated within the interlaminar zones (IZs) of the dLGN, regions distinguished by dense binding of Wisteria floribunda agglutinin (WFA). To determine the synaptic targets of thalamocortical axon collaterals, we examined RLD profiles in the PGN and dLGN in tissue stained for GABA. For the PGN, we found that all RLD profiles make synaptic contacts with GABAergic PGN somata, dendrites, and spines. In the dLGN, RLD profiles primarily synapse with GABAergic dendrites that contain vesicles (F2 profiles) and non-GABAergic dendrites in glomerular arrangements that include triads. Occasional synapses on GABAergic somata and proximal dendrites were also observed in the dLGN. These results suggest that correlated dLGN activity may be enhanced via direct synaptic contacts between thalamocortical cells, whereas noncorrelated activity (such as that occurring during binocular rivalry) could be suppressed via thalamocortical collateral input to PGN cells and dLGN interneurons.     

The dorsal lateral geniculate nucleus of macropodid marsupials: cytoarchitecture and retinal projections

The anatomy of the dorsal lateral geniculate nucleus (LGd) is described in five macropodid species, including two rat kangaroos (bettong and potoroo), two wallabies (pademelon and tammar), and the large grey kangaroo. The distribution of retinal terminals in the LGd was examined following intraocular injections of tritiated amino acids. There are considerable differences in both LGd cytoarchitecture and the patterns of retinal terminations among the five species. Cytoarchitecture in the bettong LGd is relatively simple, displaying a minimal regional differentiation. In contrast, the potoroo LGd is quite complex and displays several well-defined cell laminae, each of which is associated with input from a single eye. Both rat kangaroos display the same basic pattern of retinal termination with three bands of terminals from the contralateral eye and four from the ipsilateral eye. The bands are less sharply defined in the bettong, in which terminals from each eye overlap to a greater extent than is seen in the potoroo. The wallabies and kangaroos display a more complex LGd architecture and patterning of retinal terminal bands. Bilateral retinal projections within the same LGd lamina are unusual in these large macropodids. The number of terminal bands reaches ten in the grey kangaroo--four from the contralateral eye and six from the ipsilateral eye. The pademelon LGd is unusual in that it shows intraspecies variation with some animals displaying five ipsilateral terminal bands and others only four. The results are discussed in comparison with the patterns of LGd organisation observed in other mammalian lines, placental and marsupial. We conclude that LGd lamination and the segregation of retinal inputs to the LGd in marsupials are likely to be the result of evolutionary factors which differ from those which have produced ocular segregation and complex lamination in several lines of placental mammals.     

Y retinal terminals contact interneurons in the cat dorsal lateral geniculate nucleus

One of the largest influences on dorsal lateral geniculate nucleus (dLGN) activity comes from interneurons, which use the neurotransmitter gamma-aminobutyric acid (GABA). It is well established that X retinogeniculate terminals contact interneurons and thalamocortical cells in complex synaptic arrangements known as glomeruli. However, there is little anatomical evidence for the involvement of dLGN interneurons in the Y pathway. To determine whether Y retinogeniculate axons contact interneurons, we injected the superior colliculus (SC) with biotinylated dextran amine (BDA) to backfill retinal axons, which also project to the SC. Within the A lamina of the dLGN, this BDA labeling allowed us to distinguish Y retinogeniculate axons from X retinogeniculate axons, which do not project to the SC. In BDA-labeled tissue prepared for electron microscopic analysis, we subsequently used postembedding immunocytochemical staining for GABA to distinguish interneurons from thalamocortical cells. We found that the majority of profiles postsynaptic to Y retinal axons were GABA-negative dendrites of thalamocortical cells (117/200 or 58.5%). The remainder (83/200 or 41.5%) were GABA-positive dendrites, many of which contained vesicles (59/200 or 29.5%). Thus, Y retinogeniculate axons do contact interneurons. However, these contacts differed from X retinogeniculate axons, in that triadic arrangements were rare. This indicates that the X and Y pathways participate in unique circuitries but that interneurons are involved in the modulation of both pathways.     

Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat

We have made a fine structural investigation of the synaptic patterns made by axon terminals of retinal ganglion cells in the dorsal lateral geniculate nucleus of the cat. We compared the retinal input to dendritic processes that bear clusters of large appendages with the retinal input to relatively smooth dendritic segments that have only a few isolated spines. The study was restricted to the portion of laminae A and A1 that receive central visual field input. We were able to completely reconstruct 33 individual terminal boutons from long series of consecutive thin sections. Retinal terminals that were presynaptic to dendritic appendages tended to occupy the central position in the complex synaptic zones of geniculate fine structure called glomeruli. These terminals were surrounded by significantly more profiles than retinal terminals that were presynaptic to dendritic stems and averaged twice as many synaptic contacts per terminal bouton. The retinal input to dentritic appendages was heavily involved in a specific synaptic pattern called the triadic arrangement while retinal input to dendritic stems was only lightly involved in triads. Dendritic appendages in triads received greater synaptic input from profiles with flattened vesicles than did the dendritic stems that were found in triads.     

Complex convolutions in neurons of the dorsal lateral geniculate nucleus of the normal albino rat

The postnatal development of complex convolutions (CCs) of the dorsal lateral geniculate nucleus (LGNd) in normal rats has been studied quantitatively with light microscopy. We report that immature neurons do not contain these scarcely understood organelles, since they can be seen for the first time in very few, mature neurons of the 30 day rat; their number constantly increases during the following 4 months. These cytoplasmic inclusions can be equally seen in the aged rat. CCs are present in neurons of all sizes, except the smallest, which correspond to the interneuron population. Although, morphologically, CCs of the LGNd of the rat are similar, but not identical, to the cytoplasmic multilaminated bodies of the cat, intermediate forms are described.     

The organization of retinal maps within the dorsal and ventral lateral geniculate nuclei of the rabbit

The cytoarchitectonic subdivisions in the rabbit's dorsal and ventral lateral geniculate nuclei have been related to the several retinal maps that can be defined in terms of the distribution of retinal axons within these nuclei. Destruction of different retinal sectors was combined with intravitreal injections of ³H-proline, so that the distribution of fiber degeneration and autoradiographic label in the geniculate nuclei could be used to define the retinal maps in each nucleus, and to compare the two nuclei with each other. The two nuclei show surprisingly similar patterns of organization. Each is made up of a laminated alpha sector that curves around a relatively cell-sparse beta sector. Two morphologically distinct layers of each alpha sector receive contralateral retinal afferents and between these there is a small region in receipt of ipsilateral afferents. In each nucleus, the lines of projection that represent single points in visual space pass perpendicular to the layers of the alpha sector and continue an almost straight course into the beta sector. Quantitative comparisons of the retinal maps show that the relative volumes devoted to the representation of segments of the visual field are approximately the same in the two nuclei.     

Distribution of morphologically different retinal axon terminals in the hamster dorsal lateral geniculate nucleus

Afferent terminal arbors in the hamster LGBd were labelled with horseradish peroxidase (HRP) implanted into the optic tract. Three morphologically distinct terminal types, each with a different regional distribution, were observed. Type R1 terminals are large, ovoid swellings and are predominantly distributed medially within the nucleus. Type R2 terminals are very small, clustered varicosities and are distributed laterally and ventrally. Type R3 terminals are medium in size and their distribution overlaps with that of Type R1 and R2 terminals.     

Serotonergic inhibition of the dorsal lateral geniculate nucleus

Electrophysiological studies were conducted on chloral hydrate-anesthetized rats to determine if the dorsal raphe nucleus (DR) exerts an inhibitory influence upon the dorsal lateral geniculate nucleus (dLGN), and if this inhibition is mediated by the release of serotonin (5-HT). Conditioning stimuli presented to the DR 100-400 ms before an optic tract (OT) shock significantly lowered the amplitude of OT shock-elicited, postsynaptic, field potentials of less than 3 ms latency. Rare, long-latency, field potentials (greater than 5 ms) were diminished in amplitude when preconditioning intervals were less than 15 ms. Six days after intracerebral injection of the 5-HT neurotoxin, 5,7-dihydroxytryptamine (8 micrograms), into the dLGN, significant reductions were observed in 5-HT and 5-hydroxyindole acetic acid in the dLGN. Field potentials recorded on the sixth day in indoleamine-depleted dLGN were significantly less inhibited by DR preconditioning. Intracerebral injections of a control solution neither altered monoamine levels nor the degree of inhibition by DR preconditioning. These data provide further evidence that inhibition of dLGN by DR is mediated by release of 5-HT.     

The organization of the lateral geniculate nucleus and of the geniculocortical pathway that develops without retinal afferents

The fine structure and cortical connections of the dorsal lateral geniculate nucleus have been studied in postnatal (3.5-14-month-old) ferrets in which all retinal afferents had been removed prenatally at the time these fibers are first starting to invade the nucleus. The synaptic profiles in the mature nucleus show the cytological characteristics and arrangements that would remain if the retinal afferents were removed, with no significant compensatory ingrowth of foreign specific afferents. The nucleus is reduced in overall volume, but the geniculocortical and corticogeniculate interconnections show an essentially normal topography. Although in these experiments the geniculocortical projections can establish a normal topographic pattern in the absence of retinal afferents an accompanying paper shows that this topographic pattern can also be modified in the presence of abnormal retinogeniculate inputs. We conclude that two separate mechanisms contribute to the formation of retinal maps within the geniculocortical pathways and that different interactions between these two mechanisms produce the different patterns of abnormal geniculocortical pathways that have been described in pigment-deficient cats, mink and ferrets.     

The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat

The structural features of corticogeniculate axons were studied in adult cats after labeling them with horseradish peroxidase (HRP). Injections of HRP into the optic radiations near the dorsal lateral geniculate nucleus result in Golgi-like filling of both geniculate relay neurons and corticogeniculate axons. In the present material at least two main types of axons could be defined. The most common type is called the type I axon because it so closely resembles the type I axons described by Guillery ('66, '67) in Golgi preparations. These fine axons have smooth surfaces and consistent fiber diameter. Most terminal swellings are at the ends of short collateral branches and these swellings form asymmetric synaptic contacts onto small and medium-sized dendrites. Type I axons typically innervate more than one lamina as well as interlaminar zones and they clearly arise from the cerebral cortex. The second type of axon is called the beaded axon because of its numerous swellings, en passant. These swellings frequently are larger than those on type I axons and they differ from previously described corticogeniculate axon terminals in their ultrastructural features. That is, their synaptic contacts appear symmetrical and they form axosomatic contacts. Because of these differences, the possibility that beaded axons are of subcortical origin, particularly from the perigeniculate nucleus, is discussed. When type I axons and geniculate relay neurons are filled in the same region of the nucleus it is possible to identify probable sites of synaptic contact by using the light microscope. Such analyses indicate that corticogeniculate axons synapse directly onto relay cells, primarily on peripheral dendritic branches. Further, it appears that single axons contact many geniculate neurons and that single neurons are contacted by many axons.