Y-cell Pathway Research Articles

Immediate Impact of Acute Elevation of Intraocular Pressure on Cortical Visual Motion Processing.

PurposeTo physiologically examine the impairment of cortical sensitivity to visual motion during acute elevation of intraocular pressure (IOP).MethodsMotion processing in the cat brain is well characterized, its X and Y cell visual pathways being functionally analogous to parvocellular and magnocellular pathways in primates. Using this model, we performed ocular anterior chamber perfusion to reversibly elevate IOP over a range from 30 to 90 mm Hg while monitoring cortical activity with intrinsic signal optical imaging. Drifting random-dot fields and gratings were used to characterize cortical population responses to motion direction and orientation in early visual areas 17 and 18.ResultsWe found that acute IOP elevations at 50 mm Hg and above, which is often observed in acute glaucoma, suppressed cortical motion direction responses. This suppression was more profound in area 17 than in area 18, and more profound in central than peripheral visual field (eccentricities 0°–4° vs. 4°–8°) within area 17. In addition, orientation responses were more suppressed than motion direction responses for the same IOP modulation.ConclusionsIn contrast to human chronic glaucoma that may cause greater dysfunction in large-cell magnocellular than in small-cell parvocellular visual pathways, our direct measurement of cortical processing networks implies that the small X-cell pathway shows greater vulnerability to acute IOP elevation than the large Y-cell pathway in visual motion processing. The results demonstrate that fine discrimination mechanisms for motion in the central visual field are particularly impacted by acute IOP attacks, suggesting a neural basis for immediate visual deficits in the fine motion perception of acute glaucoma patients.

Nonlinear Y-Like Receptive Fields in the Early Visual Cortex: An Intermediate Stage for Building Cue-Invariant Receptive Fields from Subcortical Y Cells.

A significant fraction of neurons in early visual cortex have specialized receptive fields that allow them to selectively respond to the orientation of boundaries that are invariant to the cue (luminance, contrast, texture, motion) that defines them. However, the neural mechanism to construct such versatile receptive fields remains unclear. Using multielectrode recording, we found a large fraction of neurons in early visual cortex with receptive fields not selective for orientation that have spatial nonlinearities like those of subcortical Y cells. These are strong candidates for building cue-invariant orientation-selective neurons; we present a neural circuit model that pools such neurons in an imbalanced "push-pull" manner, to generate orientation-selective cue-invariant receptive fields.

Lack of early pattern stimulation prevents normal development of the alpha (Y) retinal ganglion cell population in the cat

Binocular deprivation of pattern vision (BD) early in life permanently impairs global motion perception. With the SMI-32 antibody against neurofilament protein (NFP) as a marker of the motion-sensitive Y-cell pathway (Van der Gucht et al. [2001] Cereb. Cortex 17:2805-2819), we analyzed the impact of early BD on the retinal circuitry in adult, perceptually characterized cats (Burnat et al. [2005] Neuroreport 16:751-754). In controls, large retinal ganglion cells exhibited a strong NFP signal in the soma and in the proximal parts of the dendritic arbors. The NFP-immunoreactive dendrites typically branched into sublamina a of the inner plexiform layer (IPL), i.e., the OFF inner plexiform sublamina. In the retina of adult BD cats, however, most of the NFP-immunoreactive ganglion cell dendrites branched throughout the entire IPL. The NFP-immunoreactive cell bodies were less regularly distributed, often appeared in pairs, and had a significantly larger diameter compared with NFP-expressing cells in control retinas. These remarkable differences in the immunoreactivity pattern were typically observed in temporal retina. In conclusion, we show that the anatomical organization typical of premature Y-type retinal ganglion cells persists into adulthood even if normal visual experience follows for years upon an initial 6-month period of BD. Binocular pattern deprivation possibly induces a lifelong OFF functional domination, normally apparent only during development, putting early high-quality vision forward as a premise for proper ON-OFF pathway segregation. These new observations for pattern-deprived animals provide an anatomical basis for the well-described motion perception deficits in congenital cataract patients.

Subcortical Representation of Non-Fourier Image Features

A fundamental goal of visual neuroscience is to identify the neural pathways representing different image features. It is widely argued that the early stages of these pathways represent linear features of the visual scene and that the nonlinearities necessary to represent complex visual patterns are introduced later in cortex. We tested this by comparing the responses of subcortical and cortical neurons to interference patterns constructed by summing sinusoidal gratings. Although a linear mechanism can detect the component gratings, a nonlinear mechanism is required to detect an interference pattern resulting from their sum. Consistent with in vitro retinal ganglion cell recordings, we found that interference patterns are represented subcortically by cat LGN Y-cells, but not X-cells. Linear and nonlinear tuning properties of LGN Y-cells were then characterized and compared quantitatively with those of cortical area 18 neurons responsive to interference patterns. This comparison revealed a high degree of similarity between the two neural populations, including the following: (1) the representation of similar spatial frequencies in both their linear and nonlinear responses, (2) comparable orientation selectivity for the high spatial frequency carrier of interference patterns, and (3) the same difference in their temporal frequency selectivity for drifting gratings versus the envelope of interference patterns. The present findings demonstrate that the nonlinear subcortical Y-cell pathway represents complex visual patterns and likely underlies cortical responses to interference patterns. We suggest that linear and nonlinear mechanisms important for encoding visual scenes emerge in parallel through distinct pathways originating at the retina.

The Smooth Monostratified Ganglion Cell: Evidence for Spatial Diversity in the Y-Cell Pathway to the Lateral Geniculate Nucleus and Superior Colliculus in the Macaque Monkey

In the primate visual system approximately 20 morphologically distinct pathways originate from retinal ganglion cells and project in parallel to the lateral geniculate nucleus (LGN) and/or the superior colliculus. Understanding of the properties of these pathways and the significance of such extreme early pathway diversity for later visual processing is limited. In a companion study we found that the magnocellular LGN-projecting parasol ganglion cells also projected to the superior colliculus and showed Y-cell receptive field structure supporting the hypothesis that the parasol cells are analogous to the well studied alpha-Y cell of the cat's retina. We here identify a novel ganglion cell class, the smooth monostratified cells, that share many properties with the parasol cells. Smooth cells were retrogradely stained from tracer injections made into either the LGN or superior colliculus and formed inner-ON and outer-OFF populations with narrowly monostratified dendritic trees that surprisingly appeared to perfectly costratify with the dendrites of parasol cells. Also like parasol cells, smooth cells summed input from L- and M-cones, lacked measurable S-cone input, showed high spike discharge rates, high contrast and temporal sensitivity, and a Y-cell type nonlinear spatial summation. Smooth cells were distinguished from parasol cells however by smaller cell body and axon diameters but ∼2 times larger dendritic tree and receptive field diameters that formed a regular but lower density mosaic organization. We suggest that the smooth and parasol populations may sample a common presynaptic circuitry but give rise to distinct, parallel achromatic spatial channels in the primate retinogeniculate pathway.

Postnatal dendritic development of Y-like geniculocortical relay neurons

We describe the dendritic development of neurons in the dorsal lateral geniculate nucleus (LGNd) projecting to cortical area 18 in the postnatal cat. LGN neurons were identified by retrograde labeling from area 18 with fluorescent latex microspheres and injected in the fixed slice with Lucifer yellow (LY) and horseradish peroxidase (HRP) to visualize their dendritic arborizations. Both topological (measures of the patterns of dendritic branching and their territorial coverage) and metric parameters (measures of the quantitative parameters describing the size, length, extent and diameter of the dendritic arbors) were measured in three-dimensions for 25 LGN neurons in cats between 1 and 18 postnatal weeks. In addition, dendritic growth was compared to the changing dimensions of the LGNd. At all ages, neurons projecting to area 18 have large somata and radiate dendrites. From 1 to 18 weeks neurons increase in size—both soma area and the length of all dendritic segments double during this period. Intermediate and terminal dendritic segments show comparable growth until 5 weeks. However, only terminal segments continue to grow significantly from 5 until 18 weeks. Dendrites become straighter during development, the angle between daughter branches decreases and dendritic segment diameter increases, with terminal segments showing a greater increase relative to intermediate segments. The density of dendritic appendages increases transiently at 5 weeks and a differential redistribution occurs, so that by 18 weeks dendrites further from the soma have a greater density of appendages than those near the soma. Some dendritic relationships remain invariant during development—intermediate segments are always shorter, thicker and straighter than terminal segments. During these changes however, area 18 projecting neurons maintain a constant number of primary dendrites and have, on average, a constant branching pattern. The relative volume of the LGNd occupied by an area 18 projecting neuron increases 2.4-fold between 1 and 18 weeks as the dendrites grow with the result that the coverage of a given point of the LGNd by dendrites of area 18 projecting nearly doubles from 24 to 45 neurons per unit volume. This increased net dendritic overlap provides a substrate for enhanced numerical synaptic divergence of the Y-cell pathway from a point source in the retina to the visual cortex.

Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly

In dipteran insects, the lobula plate neuropil provides a major efferent supply to the premotor descending neurons that control stabilized flight. The lobula plate itself is supplied by two major parallel retinotopic pathways from the medulla: small-field, magnocellular afferents that are implicated in achromatic motion processing and Y cells that connect the medulla with both the lobula plate and the lobula. A third pathway from the medulla involves transmedullary (Tm) neurons, which provide inputs to palisades of small-field neurons in the lobula. Although, in their passage to the brain, many output neurons from the lobula plate are separated physically from their counterparts in the lobula, there is an additional class of lobula complex output neurons. This group is composed of retinotopic lobula plate-lobula (LPL) and lobula-lobula plate (LLP) cells, each of which has dendrites in both the lobula and the lobula plate. The present account describes the anatomy and physiology of exemplars of LPL and LLP neurons, a wide-field tangential neuron that is intrinsic to the lobula complex, and representatives of the Tm- and Y-cell pathways. We demonstrate novel features of the lobula plate, which previously has been known as a motion-collating neuropil, and now also can be recognized as supporting direction- or nondirection-specific responses to local motion, encoding of contrast frequency, and processing of local structural features of the visual panorama.

Synaptic circuitry of physiologically identified W-cells in the cat's dorsal lateral geniculate nucleus

The cat's retinogeniculocortical system is comprised of at least 3 parallel pathways, the W-, X-, and Y-cell pathways. Prior studies, particularly at the level of the lateral geniculate nucleus, have focused on X- and Y-cells. In the present study, we describe the synaptic inputs for 2 geniculate W-cells from the parvocellular C-laminae after these neurons were physiologically identified and intracellularly labeled with HRP. For each of the W-cells, we examined electron micrographs taken from over 500 consecutive thin sections; we reconstructed the entire soma plus roughly 15% of the dendritic arbor and determined the pattern of synaptic inputs to these reconstructed regions of each neuron. In several ways, each W-cell exhibits a similar pattern of synaptic inputs. First, we estimate that each W-cell receives approximately 3000-4000 synaptic contacts, which occur most densely on dendrites 50-150 microns from each soma. Second, axosomatic contacts are extremely rare, and most derive from terminals with flattened or pleomorphic vesicles (F terminals). Third, terminals with round vesicles, large profiles, and pale mitochondria (RLP terminals), which are presumed to be retinal terminals, form only about 2-4% of all synapses onto these W-cells; these synapses occur on proximal dendrites. Fourth, F terminals, which provide roughly 15-20% of all synaptic input to these cells, occupy the same region of proximal dendritic arbor as do the RLP terminals. Fifth, and finally, terminals with round vesicles, small profiles, and dark mitochondria (RSD terminals) provide the majority of synapses along all portions of the dendritic arbor. Compared with geniculate X- and Y-cells of the A-laminae (Wilson et al., 1984), these W-cells are innervated by fewer synapses overall and, in particular, by dramatically fewer synapses from RLP (or retinal) terminals. This paucity of direct retinal input to geniculate W-cells might explain the remarkably poor responsiveness of these neurons to visual stimuli and to electrical activation of the optic chiasm.

Morphology and physiology of single neurons in the medial interlaminar nucleus of the cat's lateral geniculate nucleus

Physiological studies have shown that the cat's retinogeniculocortical system is comprised of at least three parallel and independent pathways, the W-, X-, and Y-cell pathways. The morphological correlates of the constituent W-, X-, and Y-cells have been determined both in the retina and in the A and C laminae of the lateral geniculate nucleus. The aim of this study was to extend these structure/function relationships to neurons in laminae 1 and 2 of the medial interlaminar nucleus (MIN), which is a division of the cat's dorsal lateral geniculate nucleus. We used intracellular injection of horseradish peroxidase (HRP) into individual, physiologically identified MIN neurons. Since this procedure may yield an unrepresentative sample of MIN neurons, two controls were performed. First Nissl staining showed that the soma sizes of intracellularly labeled cells were representative of those of all MIN cells. Second, retrograde labeling following HRP injections into the optic radiations or specific visual cortical areas showed that the intracellularly labeled MIN cells were representative of MIN relay neurons. Many of the retrogradely labeled cells were so well filled that their entire dendritic arbors were revealed. Of 70 MIN neurons recorded physiologically, 22 were injected with HRP and successfully recovered. We also completely labeled the somata and dendrites of 114 MIN neurons from HRP injections into the optic radiations and retrogradely labeled 165 MIN neurons by injection of HRP into visual cortical areas. Our sample of intracellularly injected neurons, which were all Y-cells, were morphologically representative of all MIN relay cells. We thus conclude that laminae 1 and 2 of the MIN contain a nearly homogeneous population of Y-cells with properties essentially identical to those of Y-cells in the A and C laminae of the lateral geniculate nucleus. When viewed in the coronal plane, MIN projection neurons typically exhibited oval or elongated somata. In the medial and ventral parts of the MIN, these somata were smaller and more flattened. MIN soma sizes extended over the full range of those seen in the A laminae. Dendritic arbors of most MIN relay neurons radiated in a fairly spherical fashion. In the medial and ventral parts of the MIN, however, dendrites were oriented in a more bipolar fashion, but intermediate forms between spherical and bipolar arbors were also common. Dendrites of MIN projection neurons were typically smooth; most primary dendrites were straight, but secondary dendrites were more variable in structure.(ABSTRACT TRUNCATED AT 400 WORDS)

Cat lateral suprasylvian cortex: Y-cell inputs and corticotectal projection.

Retinal Y-cells activate most cells in the deep layers of the cat's superior colliculus via an indirect pathway involving the occipital cortex. The lateral suprasylvian area seems to be an important source of visual input to the deep collicular strata but it is unclear whether Y-cell influences reach this extrastriate area and, hence, whether this area participates in the indirect Y-cell pathway. In this study, retinal influences on the posteromedial lateral suprasylvian area (PMLS) were studied in anesthetized cats. Responses to electrical stimulation of the optic disk (OD) and optic chiasm (OX) were recorded in single units in PMLS and in neurons of the dorsal lateral geniculate nucleus (LGNd) that were antidromically driven from PMLS. Virtually all PMLS cells (99%; 99/100) exhibited small differences (less than or equal to 0.8 ms) between OD- and OX-activation latency, indicating that they were driven by a pathway originating in rapidly conducting Y-cell axons. A small number of PMLS cells (17%; 20/118) had very short activation latencies (less than or equal to 3.2 ms from OX), comparable to those of cells in areas 17 and 18 receiving monosynaptic inputs from geniculate Y-cells. Further, LGNd cells with latency behaviors typical of Y-cells could be antidromically driven from PMLS, confirming that geniculate Y-cells project directly to PMLS. Most PMLS cells (83%; 98/118), though exhibiting small OD-OX latency differences, had absolute latencies too long to be attributed to direct inputs from geniculate Y-cells (3.3-8.5 ms from OX). Thus Y-cells in the LGNd influence most PMLS cells by way of a multisynaptic pathway. PMLS cells antidromically activated from the superior colliculus were driven only by this multisynaptic Y-cell input. Total conduction time from the retina through PMLS to the colliculus corresponds closely to the latency of the indirect Y-cell activation observed in the deep collicular layers. These results support the view that the lateral suprasylvian cortex constitutes an important source of visual input to the cat's deep collicular layers and, more generally, that the extrastriate visual cortex may figure prominently in the cortical control of gaze.

Development of X- and Y-cell retinogeniculate terminations in kittens.

The cat retinogeniculocortical pathways are organized chiefly into two parallel independent neuronal streams, one involving X-cells of the retina and lateral geniculate nucleus, and the other, Y-cells. Development of the Y-cell pathway is more seriously affected by visual deprivation than is the X-cell pathway and we reasoned that some insight into the underlying mechanisms of these effects could be gained from studies of normal development. We therefore injected horseradish peroxidase into physiologically identified X- and Y-cell retinogeniculate axons to examine the postnatal development of their terminations in kittens. As we report here, at 3-4 weeks of age, most optic tract axons can be identified physiologically as members of the X- or Y-cell class. X-cell terminal fields in lamina A or A1 are wider at 3-4 weeks than they are in adults, while Y-cell terminal fields are narrower than in adults. During the second and third postnatal months, X-cell terminal arbors progressively contract while Y-cell arbors expand so that, by 12 weeks of age, the adult pattern is seen. These data, and the results of our earlier study of the effects of monocular lid suture on these terminal arbors, suggest that enlargement of Y-cell terminations in geniculate lamina A or A1 during development may be accompanied by competitive pruning of X-cell terminations within these same laminae.

Visual cortical inputs to deep layers of cat's superior colliculus.

In the superior colliculi of cats anesthetized with ketamine, 84% of identified output cells of the deep layers could be driven by shocks to the contralateral optic disk, optic chiasm, or ipsilateral optic tract; 75% of these deep-layer cells had response latencies reflecting a polysynaptic influence of retinal Y-cells. Following large, acute lesions of the ipsilateral occipital cortex (including visual areas 17, 18, 19, and the posteromedial lateral suprasylvian area (PMLS), only 18% of deep-layer output cells were driven by electrical stimulation of the optic pathway and only 4% exhibited an indirect Y-cell influence. Thus, one or more of these visual areas may be important for the relay of retinal information, and particularly of Y-cell information, to the deep layers of the superior colliculus. This hypothesis is supported by the observation that intracortical stimulation in areas 17, 18, 19, and PMLS activated many cells of the ipsilateral, deep tectal layers at latencies consistent with those exhibited by the indirect Y-cell pathway. The distributions of activation latencies were similar to those observed in the superficial layers, raising the possibility that at least some of the cortical influence on the deep layers may be mediated by direct connections. Cells of the deep layers were more likely to be excited by a cortical stimulus that activated cells immediately above them in the superficial layers than by a stimulus that did not. This indicates that the functional connections between visual cortex and the deep collicular layers exhibit a topographic orderliness similar to that previously described for corticotectal projections to the superficial layers. These results provide further evidence that the visual cortex exerts a significant influence on cells of the deep collicular strata and that the pathways involved are capable of mediating the indirect, retinal Y-cell input to these neurons.

Monocular deprivation affects X- and Y-cell retinogeniculate terminations in cats.

The X- and Y-cell pathways in cats form two functionally distinct, parallel systems from the retina through the lateral geniculate nucleus (LGN) to the visual cortex1-4. We recently used the technique of intraaxonal injection of horseradish peroxidase (HRP) to demonstrate major differences between X- and Y-cells in their retinogeniculate termination patterns5 (compare Figs 1 alpha and 2 alpha). Normally, axons of X-cells innervate geniculate lamina A or A1 (depending on the eye of origin) in narrow zones oriented perpendicular to the lamination. Some X-cells also terminate sparsely (that is, with few boutons) in the medial interlaminar nucleus (MIN), a subdivision of the LGN. Y-cell axons terminate either in laminae C and A (from the contralateral retina) or in lamina A1 (from the ipsilateral retina) in broad zones5,6, and most also terminate densely (with many boutons) in the MIN. We now report that cats raised with monocular lid suture develop abnormal retinogeniculate termination patterns. Many X-cell axons arising from the deprived eye have unusually broad terminal fields in lamina A or A1, and some also densely innervate the MIN. Many Y-cell axons from the deprived eye have dramatically shrunken or absent terminal fields in the A laminae and MIN. These changes constitute the most peripheral effects of monocular deprivation discovered so far, are consistent with previous reports of functional abnormalities among deprived geniculate neurones4,7,8 ad suggest possible mechanisms by which the visual environment influences neuronal development.

Spatial and temporal sensitivity of normal and amblyopic cats.

1. We used the behavioral technique of conditioned suppression to measure spatial and temporal contrast sensitivity to counterphased, sine-wave gratings in eight cats. These included two normally reared cats before and after bilateral ablations of cortical area 17 and part of area 18, two cats raised in total darkness, two cats raised with binocular lid suture, and two cats raised with monocular lid suture, Visual deficits induced by cortical lesions or visual deprivation were evaluated with respect to the preoperative data of the normally reared cats. 2. The cortical lesions had virtually no qualitative effect on the cat’s visual capacities. Contrast sensitivity was reduced at higher but not lower spatial frequencies, and this can be described succinctly as a loss of spatial acuity. 3. Dark-reared and binocularly sutured cats qualitatively exhibited poorer visual capacity than that of the cortically ablated animals. The contrast sensitivity resultant from these two forms of binocular deprivation was basically similar and consisted of significant sensitivity losses at all spatial and temporal frequencies. Much more than high spatial frequencies was affected, and this amblyopia cannot be characterized simply as a spatial acuity loss. 4. Monocularly sutured cats had normal vision and contrast sensitivity with the nondeprived eye, but with the deprived eye they displayed the most severe amblyopia and poorest contrast sensitivity of any of the cats. Again, sensitivity losses were evident for all spatial and temporal frequencies, and this amblyopia is more severe than a loss of spatial acuity. 5. These psychophysical data are related to the status of W-, X-, and Y-cell pathways in these cats. Sensitivity to low spatial frequencies and integrity of the Y-cell pathway is correlated with good visual capacity. Since Y-cells are uniquely sensitive to low spatial frequencies, then the Y-cell pathway seems sufficient and perhaps necessary for reasonable visual performance. 6. Finally, because the amblyopia of normally reared cats with lesions of striate cortex is far less severe than that of the lidsutured and dark-reared cats, it follows that the constellation of deficits reported for striate cortex in these visually deprived cats cannot provide an adequate neural explanation for their amblyopia. Attempts to relate deprivation amblyopia to striate cortex abnormalities should thus be reconsidered.

The oblique effects of pattern and flicker sensitivity: implications for mixed physiological input.

The inferior contrast sensitivity for oblique gratings has been previously demonstrated at high spatial frequencies with an absolute criterion. In this study contrast sensitivity at oblique and main axis orientations was obtained under separate pattern and flicker threshold criteria across a range of both spatial and temporal frequencies. The anisotropy of contrast sensitivity was not observed at low spatial frequencies under any stimulus or criterion conditions. At high spatial frequencies the anisotropy was observed for both pattern and flicker thresholds, although the flicker anisotropy was less pronounced. If, as previously suggested, this anisotropy is mediated by X cells, then these psychophysical findings suggest a mixed model in which both pattern and flicker systems receive input from both X and Y-cell pathways.