Influence of the superior colliculus on visual responses of cells in the rabbit's lateral posterior nucleus

Summary The lateral posterior-pulvinar (LP-P) complex of mammals receives a major input from the superior colliculus (SC). We have studied the response properties of LP cells and investigated the effects of reversible inactivation of the colliculus on the visual responses of LP units in anesthetized and paralyzed rabbits. Cells in LP had large receptive fields responsive to either stationary or moving stimuli. One third of the motion-sensitive cells were direction selective. The size of the receptive fields increased with eccentricity and there was a retinotopic organization along the dorso-ventral axis. Comparison of the LP and superior colliculus properties revealed substantial differences in visual response characteristics of these two structures such as the size of the receptive fields and the number of direction-selective cells. Electrical stimulation of the LP evoked antidromic action potentials in tectal cells that were motion sensitive. We found a dorsoventral gradient in the projections of collicular cells. Units located more dorsally in the colliculus sent their axons to LP while cells lying more ventrally sent axons toward the region lying posterior to LP. A micropipette filled with lidocaine hydrochloride was lowered into the superficial layers of the superior colliculus in order to reversibly inactivate a small population of collicular cells. Rendering the superior colliculus inactive produced a sharp attenuation of visual responses in the majority of LP cells. Some neurons ceased all stimulus-driven activity after collicular blockade while a few cells exhibited increased excitability following collicular inactivation. These experiments also indicate that the tecto-LP path is topographically organized. An injection in the colliculus failed to influence the thalamic response when it was not in retinotopic register with the LP cells being recorded. Our results demonstrate that the superior colliculus input to LP is mainly excitatory in nature.     

Response properties of neurons in area 17 projecting to the striate-recipient zone of the cat's lateralis posterior-pulvinar complex: comparison with cortico-tectal cells

The main input of the lateral part of the cat's lateralis posterior-pulvinar complex (LP-P) comes from the primary visual cortex. We investigated the response properties of cells in area 17 projecting to the striate-recipient zone (LPl) of the cat's LP-P complex. The cells' receptive fields were stimulated with drifting sine-wave gratings. Cells whose fibres terminate in the superior colliculus were also recorded, to determine how their properties compare with those of cortico-LPl cells and to investigate the possibility that LPl is innervated by collaterals of cortico-tectal units. A total of 26 cells in the striate cortex were identified by antidromic activation from the LPl (mean latency 2.2 ms) and 22 from the colliculus (mean latency 2.5 ms). Only six cortical cells could be activated from the LPl and the colliculus. All cortico-LPl cells except for two responded to drifting sinusoidal gratings with unmodulated discharges (AC/DC ratios <1). On the basis of their modulation index, these units were classified as complex cells. All cortico-LPl cells were selective for the orientation of gratings (mean bandwidth of 28°). There was a tendency for cortico-LPl cells to prefer vertical and horizontal orientations. More than half of these cells (57%) were direction selective. Strong orientation anisotropies were also found in the receptive fields of cortico-tectal cells, since almost all units responded preferentially to horizontally oriented gratings. The mean preferred spatial and temporal frequencies of cortico-LPl cells were 0.74 c/deg (bandwidth 2.03 octaves) and 2.7 Hz (bandwidth 2.5 octaves), respectively. These properties did not differ significantly from those of cortico-tectal cells. Most cortico-LPl cells (72%) exhibited contrast-response curves with saturation at low contrast (mean half-saturation 0.2). For the remaining units, the responses increased linearly with contrast without clear saturation. For more than half of cortico-tectal cells (60%), the contrast function was also characterised by a response saturation. Almost all cortico-LPl cells responded to moving random dot patterns with mean tuning functions of 43.6°. Standard as well as special complex cells were found to be equally responsive to the motion of visual noise. Similar properties were recorded for cortico-tectal cells (mean bandwidth of 44.2°). Cortico-LPl and cortico-tectal cells were either binocularly or monocularly driven by the contralateral eye and their mean spontaneous firing rates were 11.7 and 10.9 spikes/s, respectively. These cells were presumably located in layer V. Stimulation of LPl and colliculus also evoked trans-synaptic responses in area 17. The average latency of the orthodromic responses from LPl was much shorter than that from the colliculus (medians 3.5 and 50 ms, respectively). The findings indicate that almost all cortico-LPl units have complex receptive fields and that their overall properties differ from those of recipient cells in LPl. These results also indicate that LPl is not likely to be innervated by collaterals of fibres of cortico-tectal cells. While cortico-LPl and cortico-tectal cells appear to form two distinct populations, there is no significant difference between the overall properties of these two cell groups.     

Relation of the parabigeminal nucleus to the superior colliculus and dorsal lateral geniculate nucleus in the hooded rat

Summary The retino-recipient layers of the superior colliculus project predominantly to the dorsal and ventral divisions of the ipsilateral parabigeminal nucleus, while receiving an input chiefly from the medial division of the contralateral nucleus. A variety of retrograde tracing techniques was used to confirm that there is a projection from the medial division of the parabigeminal nucleus to the contralateral dorsal lateral geniculate nucleus in normal adult hooded rats. Some parabigeminal cells branch to supply both dorsal lateral geniculate nucleus and retino-recipient layers of the superior colliculus.     

Evidence of a collicular input to the dorsal lateral geniculate nucleus in rabbits — electrophysiology

Summary In anesthetized and paralyzed rabbits, unit responses of lateral geniculate nucleus (LGN) cells to focal electrical stimulation of the superior colliculus were studied. Geniculate responses to collicular stimulation (SCS) were compared with responses to optic nerve shock (ONS). A weak correlation coefficient suggested that collicular stimulation did not fire geniculate cells through collateral activation. Further differentiation between collicular and retinofugal inputs to LGN was made possible by repetitive stimulation. Geniculate cells which responded to collicular stimulation were relay cells as they were antidromically invaded from the visual cortex. This ruled out recordings from the ventral geniculate, since this area does not project to the visual cortex. A direct colliculo-geniculate pathway was revealed by antidromic activation of collicular cells by stimulation of the dorsal LGN. Finally, triggering flashes by collicular firing resulted in a marked modification of the geniculate test response. The results suggest that the superior colliculus sends fibers to the LGN and is capable of modulating the retino-cortical neuronal message at the level of the LGN.     

The projection from the superior colliculus to the lateral reticular nucleus in the cat as studied with retrograde transport of WGA-HRP

Summary Medium-sized and large superior collicular neurons were retrogradely labelled after small ejections of the wheat germ agglutinin-horseradish peroxidase complex in the lateral reticular nucleus of the feline medulla. The projection from the superior colliculus to the lateral reticular nucleus is bilateral with a contralateral predominance. It originates mainly from the intermediate, but also from the deep gray layer of the superior colliculus. Our observations provide evidence that the lateral reticular nucleus is an important target of tectal efferents. The findings are discussed in relation to the organization of other fiber connections of the superior colliculus.     

The lateral cervical nucleus in the cat III. An electron microscopical study after transection of spinal afferents

Summary The ultrastructure of terminal degeneration within the lateral cervical nucleus (LCN) after transection of its spinal afferent fibers 2 days–2 years earlier is described. The degeneration after 2 days was of both the neurofilamentous and dense type. The highest number of degenerating terminals, about 15%, was found after 4–5 days. Then most of the degenerating boutons were of the dense type. The degenerating terminals had synaptic contact with cell bodies and dendrites of LCN-neurons. Removal of the degenerating boutons seemed to be effected by a phagocytic cell present in increased number compared to the normal LCN. In cases with long survival times an increase in the number of astroglial filaments was observed. In an animal where the spinal afferents to the LCN had been cut 2 years earlier a decrease in medium size of the neurons was observed. The amount of dendritic spines was also considerably smaller than normally.     

Lateral excitation in the cat lateral geniculate nucleus

Summary Visual responses were elicited by global phase reversal stimuli in cells of the cat dorsal lateral geniculate nucleus (dLGN) after small retinal lesions had been centered on each receptive field. After acute lesions of different sizes exclusively lateral inhibition was found. When GABAergic inhibition was blocked by continuous microiontophoretic application of bicuculline lateral excitation emerged in dLGN cells partially deafferented by small and medium size acute retinal lesions, but not in those affected by large lesions. This indicates the presence of excitatory retinal inputs at the periphery of the dLGN cell dendrites which are normally suppressed by strong, long-ranging lateral inhibitory processes. After chronic deafferentation, the remaining excitatory inputs increase in effectiveness and lateral excitation is seen without blockade of inhibition. The maximal lateral spread of excitation (300 m) in the dLGN is distinctly smaller than the extent of lateral inhibition (1000 m).     

Dark adaptation and receptive field organisation of cells in the cat lateral geniculate nucleus

Summary The receptive fields of LGN cells were investigated with stationary light and dark spot and annulus stimuli. Stimulus size and background intensity were varied while stimulus/background contrast was kept constant.The speed of dark adaptation varied considerably from cell to cell. Dark adaptation made responses more sustained in all neurones and eliminated the oscillatory on-responses evoked under some conditions in the light-adapted cells. Dark adaptation led also to a disappearance of early phasic inhibition in on-responses, and increased response rise time and latency.The power of surround responses to inhibit centre responses decreased slightly at low levels of light adaptation in LGN cells but much less than in retinal ganglion cells. Some other traces of changing retinal surround effects also appeared in the LGN on dark adaptation. For example, the functional size of receptive fields increased at low levels of illuminance as has been observed in retinal ganglion cells and the receptive fields as estimated from response peaks were larger than those estimated from sustained components.Trainee of the European Training Programme in Brain and Behaviour Research, 1975.     

Postnatal growth of the dorsal lateral geniculate nucleus of the cat

Summary The postnatal growth of the dorsal part of the lateral geniculate nucleus (LGNd) is studied in paraffin sections through the brains of 32 cats of known age. The changes in shape and position of the LGNd are described and it is shown that its volume increases from about 3.4 mm³ at birth to about 26.4 mm³ in the adult cat. When this value is corrected for shrinkage, the volume of the LGNd in the adult cat turns out to be about 44 mm³. The detailed measurements reveal that during the second and third week of postnatal life there is a particularly steep increase in volume and that the final values are already reached at around the 40th day. Concomitant with the increase in volume there is a decrease of the number of cells per unit volume of grey matter. In the binocular segment of lamina A the number of cells decreases from about 470 per (0.1 mm)³ at birth to between 95 and 130 per (0.1 mm)³ in the adult cat. Separate measurements of nerve cells and neuroglial cells indicate that the absolute number of nerve cells remains fairly constant during postnatal life, whereas between the second and sixth week a great number of neuroglial cells are newly formed.Dedicated to Professor W. Bargmann, Kiel, on the occasion of his seventieth birthday     

Binocular interaction in the dorsal lateral geniculate nucleus of the cat

Summary We have investigated binocular interaction in the dorsal lateral geniculate nucleus (LGN) of the cat. Neurons were recorded extracellularly during visual stimulation with sinusoidal gratings which were presented at different interocular phases (disparities). The large majority of cells (91%) exhibited some type of binocular interaction. For 75% and 16% of the total number of cells, the binocular interaction was inhibitory or facilitatory, respectively. For the remaining 9% of cells, no interaction was evident. In marked distinction from visual cortex, the facilitatory and inhibitory interactions in the LGN are independent of the relative interocular phase of the patterns. Neurons in the LGN are therefore insensitive to the stereoscopic depth cue, retinal disparity.     

Control of recurrent inhibition of the lateral geniculate nucleus by afferents from the superior colliculus of the rabbit: a possible mechanism of saccadic suppression

Summary Stimulation of the ipsilateral superior colliculus elicited a short burst of discharges of the recurrent inhibitory interneurones in the geniculocortical pathway of the rabbit. The most effective stimulating sites for this excitation were located in the deep layers rather than the superficial layers of the superior colliculus. The short latency of the response (2.3±0.6 ms) implied an oligo-synaptic excitatory pathway from the deep layers of the superior colliculus to the recurrent interneurones located in the caudal reticular nucleus of the thalamus. Following the excitation of the inter-neurone, there was a prolonged inhibition which started 10–30 ms and ended 150 ms after the collicular stimulation. The maximal inhibition occurred 50–70 ms after the stimulation. The effects of collicular stimulation on the recurrent inhibitory interneurones may be concerned with the inhibition of the visual pathway during saccades and with the disinhibition of facilitation during fixation of a new visual target.     

猫外侧膝状体神经元HRP示踪结合Calbindin的免疫组织化学研究

目的 HRP示踪结合Calbindin双标猫外侧膝状体核(LGN)至视皮质的中继神经元.方法 在猫视皮质的17区多点微量注射30%HRP,逆行标记LGN至视皮质的中继神经元,先以金标抗HRP-抗孵育切片,用免疫金银法将HRP颗粒转化黑色银颗粒.然后用ABC法作Calbindin(CB)的免疫组化,试图双标记LGN的中继神经元.结果 HRP标记细胞与CB免疫阳性细胞清晰可辨,HRP标记细胞内为银染黑色颗粒,而CB免疫阳性细胞为染色均匀的棕色.猫LGN的A、A_1和C板层均有CB免疫阳性神经元的分布;HRP标记细胞分布于A和A_1板层.LGN内未见HRP和CB的双标记神经元.结论 LGN内含CB神经元可能不参与视觉信息的传导,而是与局部视觉信息的整合有关.     

Somatotopic termination of spinal afferents to the feline lateral cervical nucleus

Summary The labelling pattern of the feline lateral cervical nucleus (LCN) was investigated after pressure injections of lectin-conjugated horseradish peroxidase into cervical, thoracic or lumbar segments of the spinal cord. Sixteen cats received a 5–8 nl injection staining large parts of mainly the ipsilateral grey matter of a single segment. Light microscopic examination of frozen sections reacted with tetramethylbenzidine showed a somatotopic organization in the LCN. Rostral segments of the spinal cord projected mainly to rostroventral and medial parts of the ipsilateral LCN, while more caudally located segments projected to more dorsocaudal and lateral parts of the nucleus. Minor contralateral labelling with a similar somatotopic arrangement was seen in animals given cervical and lumbar injections. No significant labelling was found in the LCN of three control animals, the segmental injections of which were engaged mainly into the ipsilateral dorsal columns and the dorsolateral funiculus. Ultrastructural analysis in two animals which received multiple cervical or lumbar injections showed that about 70% of the peroxidase-positive structures in the LCN were boutons and the rest small myelinated axons. The precise termination pattern of ascending afferents to the LCN is compatible with the somatotopic organization of the other relay centres in the spino-cervicothalamic pathway.     

Visual suppression from nondominant eye in the lateral geniculate nucleus: A comparison of cat and monkey

Summary We have studied the suppression of firing in single LGN cells of cat and monkey in response to visual stimulation of the nondominant eye.In the cat LGN most of the cells of each of the main laminae show this nondominat suppression. X cells having their dominant input from the ipsilateral eye were suppressed to a significantly greater degree than any other cell type in the cat LGN.In the monkey LGN nondominant suppression was absent in all 19 X-like cells studied, whereas 6 of 21 Y-like cells showed nondominant suppression. Thus nondominant suppression is present in the magnocellular laminae of the monkey LGN, where the Y-like cells are found, but appears to be absent from the parvocellular laminae, where the X-like cells are found.A preliminary report has been presented at the meeting of the Australian Physiological and Pharmacological Society in August 1977. Proc. Aust. Physiol. Pharmacol. Soc. 8, 132 (1977)     

Texture discrimination by cells in the cat lateral geniculate nucleus

Summary The spontaneous segregation of texture areas is an impressive perceptual phenomenon, the neural basis of which is not yet understood. In the texton concept (Julesz and Bergen 1983; Julesz 1984, 1986) it is assumed that the visual system analyzes a stimulus for certain features (textons) the spatial distribution of which is pre-attentively registered and may provide the percept of dissected texture areas. Supposed textons are blobs of a given size, oriented lines, line intersections and line terminators, suggesting that texture analysis is exclusively mediated by form-specific filters at higher, e.g. cortical, processing levels. This paper investigates the contribution of cells in the cat lateral geniculate nucleus (LGN) to segregation of typical texton differences. The results indicate that LGN cells, though not resembling the supposed texton filters, often distinguished textured arrangements of such features on the basis of a variety of other visual cues, such as global or local variations in mean luminance or differences in spatial frequency composition. Thus, cells responded to texture borders between areas differing in the size or the density of texture elements and often revealed differential firing rates to textures differing by the crossing or the terminator feature. For textures with differences in line orientation, however, only small variations of the firing rate were seen. In summary, the observations suggest a means of texture representation in the cat LGN which is different from recent concepts of texture segregation in man. For given pair of textures, cells with receptive fields larger than, or similar to the texture raster respond to global and local luminance variations between areas and, in particular, to differences in their spatial frequency composition. These cells, hence, may signal the global texture difference without encoding spatial details of the pattern from which texton features could be identified. Cells with receptive fields small in comparison to texture elements transfer all the information necessary for analyzing these elements in detail, but themselves are relatively insensitive to global texture differences.Supported by the Deutsche Forschungsgemeinschaft (Az.: Cr/30-14 and Cr/30-18)     

Modulations of the lateral geniculate nucleus cell responses by a second discrete conditioning stimulus: implications of the superior colliculus in rabbits

Summary This study analyzes the interactions between two discrete stimuli located in the visual field of the rabbit at the lateral geniculate level. Single unit recordings were carried out simultaneously from the superior colliculus (SC) and lateral geniculate nucleus (LGN) in anesthetized and paralyzed rabbits. A first conditioning stimulus (most often a moving target) was positioned in the receptive field of the collicular cell to ensure activation of the retino-collicular path. A second test stimulus was introduced into the receptive field of the LGN cell. The presentation of this latter stimulus was timed so as to fire the geniculate cell at various delays after the collicular neuron had responded to its own stimulus. The spontaneous firing of each cell was unaffected by the stimulus appropriate to the complementary unit. The conditioning collicular stimulus produced increases or decreases in geniculate responses. This modulation may eventually reduce the direction specificity of a geniculate unit. The fluctuations of the geniculate responses peaked 200 to 300 ms after collicular cells had responded. In a separate series of experiments the influence of the conditioning stimulus on geniculate responses was abolished when the SC was locally inactivated. These results suggest that the well documented colliculo-geniculate system mediates the interactions of several stimuli in the visual field. The outcome of this processing results in a modulation of geniculate responses.     

Projections from the lateral reticular nucleus to the cerebellar cortex and nuclei in the cat

Summary The fiber projection from the lateral reticular nucleus (LRN) to the cerebellum was examined in the cat. Electrolytic lesions were placed in a confined area of the LRN using a parapharyngeal approach, and the ensuing degeneration was studied in sections stained by the Nauta and the Fink-Heimer methods.Fibers from the LRN ascend the ipsilateral restiform body, terminating bilaterally but chiefly in the ipsilateral cerebellum. In the ipsilateral cortex projections were found to lobules I to V, with denser terminations in sublobules IVb to Ve. The projections are stronger in the intermediate-lateral zones than in the vermis proper. There is also a dense projection to sublobules VId and VIf and to the medialmost part of the simple lobule (HVI). Scanty termination was seen in the medialmost part of crus I. There is a moderate projection to the caudalmost folium of sublobule VIIb and to the rostral folia of sublobule VIIIa and the paramedian lobule. The contralateral projection by fibers crossed within the cerebellum is far less dense but clearcut in the anterior lobe, the rostral folia of lobule VI and the medial part of the simple lobule.In the ipsilateral nuclei strong projections were found to rostral portions of the medial nucleus (M) and the caudal two thirds of the anterior interpositus nucleus (IA) with predominance in the lateral part of the latter. A focal projection was found to rostrodorsal portions of the posterior interpositus nucleus (IP). No projection was found to the lateral nucleus (L). Contralaterally there is a weak projection to the rostral part of M and the medial parts of IA and IP.Abbreviations AL Anterior lobe - BP Brachium pontis - CD Subnucl. dorsalis of the nucl. medullae oblongatae centr. - CV Subnucl. ventralis of the nucl. medullae oblongatae centr. - Cr. I Crus I - Cr. II Crus II - F Flocculus - GL Granular layer - IA Anterior interpositus nucleus - IO Inferior olive - IP Posterior interpositus nucleus - LRN Lateral reticular nucleus - L Lateral nucleus - M Medial nucleus - ML Molecular layer - Pfd Paraflocculus dorsalis - Pfv Paraflocculus ventralis - Pm Paramedian lobule - RB Restiform body - SL Simple lobule - SMP Subnucleus medialis parvocellularis - ST Nucleus of the spinal trigeminal tract - XII Hypoglossal nerve nucleus     

Responses of cells in the cat lateral geniculate nucleus to moving stimuli at various levels of light and dark adaptation

Summary The responses of neurones in laminae A and A1 of the cat lateral geniculate nucleus to moving stimuli were investigated at different background luminances. Moving bright slits, dark bars and edges were employed; the contrast of stimuli against the background was held constant. Background intensities varied from 10^–3 to 10² td.Responses as stimuli passed across the centres of LGN receptive fields became stronger with increasing levels of light adaptation up to 10^–1–10¹ td and then remained constant. Responses as stimuli passed through surround regions altered qualitatively with adaptation level, generally increasing in strength and complexity with background luminance. As a bright slit for on-centre cells or dark bar for off-centre cells left the surround, in almost all units a strong secondary peak could be elicited by an appropriate selection of the adaptation conditions. Many features of the responses to moving stimuli could not be predicted from the responses to stationary stimuli under different adaptation conditions described in the previous paper.Trainee of the European Training Programme in Brain and Behaviour Research, 1975.     

The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat

Summary Cells in the cat superior colliculus which project to the ventral and dorsal lateral geniculate nuclei (VLG and DLG) have been labeled by retro-grade transport of horseradish peroxidase (HRP). We studied the depth, area, and morphology of each labeled neuron quantitatively. Our measurements show that the projection neurons to both VLG and DLG vary in laminar position, size, and morphology. Labeled cells projecting to both nuclei were concentrated within the superficial gray layer, but were also scattered through the optic layer and, after DLG injections, in the intermediate gray layer as well. Labeled cells in both groups varied greatly in size, ranging from 49–344 m² cross-sectional area (mean 143 m²) for the VLG group and from 31–398 m² (mean 165 m²) for the DLG group. The labeled cells also varied in morphology after both VLG and DLG injections. The majority had a granule or vertical fusiform morphology. There were fewer with a stellate morphology and almost none with a horizontal morphology. At least three types of superior colliculus cells thus appear to project to the ventral and dorsal lateral geniculate nuclei. These cell types likely give rise to distinct functional channels to these nuclei.Abbreviations A lamina A of the dorsal lateral geniculate nucleus - A1 lamina A1 of the dorsal lateral geniculate nucleus - C lamina C of the dorsal lateral geniculate nucleus - CM central medial nucleus - CMM medial mammillary nucleus - CP cerebral peduncle - D nucleus of Darkschewitsch - FCT central tegmental tract - H habenular nuclei - HPM medial habenulo-peduncular tract - LP lateral posterior nucleus - MG medial geniculate nucleus - MIN medial intralaminar nucleus - NCP nucleus of the posterior commissure - NR reticular nucleus - OT optic tract - P pulvinar nucleus - PC posterior commissure - R red nucleus - SG suprageniculate nucleus - SN substantia nigra - VLA ventral anterolateral nucleus - VLG ventral lateral geniculate nucleus - VPL ventral posterolateral nucleus - VPM ventral postero-medial nucleus This study was supported by USPHS Research Grant EY02973 from the National Eye Institute, a New Faculty Research Grant from the State of Tennessee, and USPHS Postdoctoral Training Grant GM-00202