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The Charles F. Prentice Award Lecture 1990: specific tests and specific blindnesses: keys, locks, and parallel processing.

Classical color vision theory incorporates the concepts of hard-wired parallel independent processing and of hard-wired opponent-processing. These two powerful concepts can be applied more generally in visual psychophysics. The concept of parallel independent processing can help to understand two extremes of visual performance: disordered vision in patients and the extraordinary visual abilities of athletes and aviators. Three illustrations of this thesis are discussed. First, evidence for dissociations of spatial vision for low-contrast and high-contrast objects. Second, evidence that a binocular system for motion in depth runs in parallel with the classical disparity-driven binocular system for relative position in depth. Third, evidence that a visual system for motion-defined form parallels the well known system for contrast-defined form. However, in principle these two concepts have limited value because they do not incorporate the possibility that the functional organization of the visual pathway could be modified by descending task-dependent signals.

Awards and Prizes↗

Online formation of a hierarchical cognitive map for object-place association by theta phase coding.

Object-place associative memory, the storage of object and place conjunctions based on a one-time experience, is hippocampal-dependent in humans. Theta phase precession, a type of neural dynamics observed in the rat hippocampus, has recently been suggested to serve a role in instantaneous memory formation based on a one-time experience, while its functional role in associating distinct types of information (object and place information) is unclear. In this study, we hypothesize that theta phase encoding with theta phase precession contributes to the storage of object-place associations. To examine this hypothesis, we propose a neural network model of the corticohippocampal system, including central-peripheral visual pathways and theta phase coding in the hippocampus. Memory storage computer experiments demonstrate that the hippocampal network successfully stores the object-place associations of a one-time experience. Interestingly, it is also found that a random visual input sequence results in a robust formation of asymmetric connections between objects and scenes instantaneously after a single trial. Furthermore, it is found that scene-object connections and scene-scene connections form a hierarchical network representing the spatial alignment of scenes and objects in the environment. Our findings indicate that the theta phase coding, as observed in the rat hippocampus, can facilitate the online memory storage of complex environments in humans as a hierarchical cognitive map.

Action Potentials↗

Region-selective decline of in vivo lipid synthesis in the aged rat visual system.

[14C]palmitate and [3H]choline were injected intravitreally and, at the same time, intraventricularly in Wistar male rats at 4, 10, and 24 mo of age. The precursor incorporation into lipids of the retina, optic nerve tract, superior colliculus, and lateral geniculate body was followed for 2 h. The specific radioactivity of precursors pool (choline, phosphorylcholine, and free fatty acids) showed a marked decrease in optic nerve tract and lateral geniculate body of aged rats, whereas in retinal tissue and superior colliculus no changes were observed as a function of age. In rats of the three age groups, whole retina and superior colliculus showed neither changes of choline incorporation into phosphatidylcholine and sphingomyelin nor alteration of palmitate incorporation into diacylglycerols, triacylglycerols, and major phospholipid classes as a function of age. In sharp contrast, the optic nerve tract and, to a lesser extent, the lateral geniculate body exhibited a significant age-related decline of either the incorporation of both precursors into all lipid classes or the specific radioactivities of endogenous precursor pools. We concluded that the visual pathway structures are metabolically affected in a different manner by aging. Particularly, the ability of the retina and superior colliculus to metabolize lipids appeared to be age invariant. The marked decline of lipid biosynthesis with age, for some visual structures, is consistent with the trend generally observed in metabolic turnover and function of other CNS regions.

Aging↗

"Let There be Light!" pigeon eggs are regularly exposed to light during breeding.

Light stimulation before hatching initiates the emergence of avian visual lateralisation. Since several studies show that birds benefit from being lateralised, we can conjecture that their clutch is being exposed to light during breeding. We tested this assumption in pigeons with a semi-natural setup where the animals were systematically recorded using a movement detection system throughout their breeding period. The results show that pigeon pairs perform their relieves in a regular way by abandoning their clutch for a mean of about 55 s at approximately every 43 min. Thus, the developing visual pathways are repetitively stimulated by light for cumulatively over 3h before the breeding period ends. It becomes apparent that both the duration as well as the repetitions of light stimulation play a crucial role in the onset of visual asymmetry.

Animals↗

Changing distribution of GABA-like immunoreactivity in pigeon visual areas during the early posthatching period and effects of retinal removal on tectal GABAergic systems.

The distribution of GABA-like immunoreactivity in the pigeon visual system was studied during the first 9 days after hatching using a mouse monoclonal antibody, mAb 3A12, to glutaraldehyde linked GABA (Matute & Streit, 1986). GABA-like immunoreactivity was seen in cell bodies as well as in neuropil at the level of both the retina and central visual regions at any posthatching age. However, the distribution of putative GABAergic cells and processes varied with age reaching the adult pattern at around 9 days. As a general observation, almost no cell bodies in the retina (except for some perikarya in the ganglion cell layer) were labeled at hatching but densely packed immunostained processes were present in the inner plexiform layer. During the next few days, GABA-immunoreactive amacrine and horizontal cells appeared and the adult distribution of GABA-like immunoreactivity was reached at around 9 days. In the other visual regions examined, the general trend in the variation of GABA-like immunoreactivity included: (1) a progressive decrease in the density of immunostained cell bodies and (2) an almost parallel increase in the concentration of stained neuropil. Since in pigeons the adult organization of visual pathways and the final distribution of putative GABAergic systems are reached at around the same age, we suggest the possibility that incoming ganglion cell axons play a role in regulating the distribution of GABA-like immunoreactivity in visual areas. This hypothesis is supported by the fact that the distribution of GABA-like immunoreactivity in the superficial layers of the optic tectum was altered following ablation of the contralateral retina immediately after hatching.

Animals↗

Structure of physiologically classified neurones in the kitten dorsal lateral geniculate nucleus.

The mammalian forebrain, including the dorsal lateral geniculate nucleus (LGNd) and the visual cortex, continues both structural and functional development postnatally and is therefore a useful model for the study of developmental processes in the central nervous system (CNS). We report here the first description and comparison of the structural development of individual, functionally identified neurones in the mammalian forebrain. This comparison is made for the three main cell groups of the central visual pathways (W-, X- and Y-cells), in the neonate and the adult. In the adult, these three classes of neurones have different characteristic electrophysiological properties(1-9) and relay information in parallel about different features of a visual scene8,9 from the retina through the LGNd to the visual cortex. In addition, each of the three functional cell types has a characteristic structure in the adult10,11. By injection of the enzyme marker substance, horseradish peroxidase, into electrophysiologically identified neurones, the present study demonstrates that each of these functional classes of neurones also has a characteristic morphology in the neonate (in the LGNd of kitten 3-4 postnatal weeks of age). However, striking differences in the rates of maturation are seen. The W-cells are already mature at this age. The X-cells are the least developed. Surprisingly, some Y-cells are mature. Due to the susceptibility of Y-cells to an abnormal visual environment during development12-18, they had previously been thought to be slower to mature.

Animals↗

Neuroimaging in children with congenital disorders of the peripheral visual system.

The study investigates the neurological substrate in children with congenital disorders of the peripheral visual system (CDPVS), i.e. disorders of the anterior visual pathways and the globe. The design is retrospective; brain MRI and/or CT scans were traced and reviewed for 79 of 254 children with CDPVS on our database. The neuroradiological findings were considered in the context of degree of visual impairment (profound [PVI] and severe [SVI]), developmental outcome (setback and non-setback), and mode of imaging (MRI and CT). Scans were abnormal in 40 of 79 (51%) children; 23 of 40 (58%) had more than one lesion; and in some children lesions not previously reported were found. The number of abnormalities per child was significantly higher in the PVI than the SVI group (P<0.05); the level of significance varied according to the method of scanning (MRI, P<0.001; CT, ns). Seven children were known to have had developmental setback; significantly more brain abnormalities per child were found in the group with setbacks than in the group without (P<0.001). Eighty-six percent (24 of 28) of MRI compared with 38% (22 of 58) of CT scans were abnormal. MRI detected more lesions per child than CT (P< 0.001). Thus, a significant amount of brain pathology occurs in children with CDPVS. The number of lesions varies directly with degree of visual impairment and both correlate with developmental outcome. As brain pathology will be only one of many factors influencing developmental progress in visually impaired children, prospective multifactorial studies of the CDPVS population, which include MRI studies of the neurological substrate, will be required to clarify the latter.

Brain↗

Conditioned and unconditioned aversive stimuli enhance light-induced fos expression in the primary visual cortex.

Studies in rats indicate that photic responses within the dorsal lateral geniculate nucleus can be enhanced in response to stimuli known to induce negative emotional arousal. Little is known, however, about the effect of such stimuli on photic responses within primary visual cortex, the principal projection area of the dorsal lateral geniculate. Here, we examined the effect of unconditioned and conditioned aversive stimuli on photic responses within the primary visual cortex in rats using expression of the transcription factor Fos as a functional marker of neuronal activation. In previous studies carried out within the circadian visual system, we found that photic induction of Fos within the principal target area of the circadian visual pathway, the suprachiasmatic nucleus of the hypothalamus, was attenuated when the light stimulus was given concurrently with an aversive footshock or was made an aversive conditioned stimulus through previous pairings with footshock. In addition, we found that photic stimulation of Fos expression in the suprachiasmatic nucleus was attenuated in a context made aversive through previous pairings with footshock. We now report that in these same animals, unlike what was seen within the suprachiasmatic nucleus, Fos expression in the primary visual cortex is significantly elevated. These findings support the view that emotional arousal can enhance the response of cells in the visual cortex to photic input, and point to the differential effect of aversive emotional events on photic responses within pathways underlying visual perception and those involved in circadian regulation.

Animals↗

Simple and complex retinal ganglion cell axonal rearrangements at the optic chiasm.

The rearrangements that retinal ganglion cell (RGC) axons undergo near the optic chiasm were determined by ablating either the nasal, temporal, dorsal, ventral, or peripheral retina. The axons of the remaining intact RGCs were then labelled with cobaltous lysine. RGC axons change their relationship with respect to the axes of the brain and with respect to one another. Toward the caudal end of the optic chiasm, the optic tract begins to rotate axially such that its rostral edge ultimately becomes located medially. Thereby, the column of ventronasal RGC axons shifts from a rostral to a medical position. In addition, columns of axons from other retinal sectors move with respect to one another. Ventrotemporal RGC axons, located initially at the caudal edge of the tract, move toward and come to be positioned laterally to, the column of ventronasal RGC axons. The column of dorsonasal RGC axons moves from the rostral to the lateral side of the column of dorsotemporal RGC axons. Concurrently, the axons within each column reorganize internally. Each chronological lamina of axons within a column twists such that the nasal and temporal axons within each column invert their positions with respect to the edges of the column. All of these reorganizations take place between the caudal end of the optic chiasm and the division of the main optic tract into the optic brachia. Furthermore, the rearrangements that occur do not involve any alterations in the positions of central and peripheral RGC axons with respect to the surface of the diencephalon. The results are discussed with respect to mechanisms that might influence the organization of the visual pathways.

Animals↗

Development of retinohypothalamic projections in the chick embryo.

The retinal projection to the hypothalamus was investigated in embryonic as well as hatched chick using wheat germ agglutinin-conjugated horseradish peroxidase as an anterograde tracer. The presence of an aggregation of anterogradely labeled terminals in the hypothalamus was used to identify the suprachiasmatic nucleus (SCN). The first clear labeling of retinal fibers in the SCN was found on embryonic day 16, whereas labeling was found in the other primary visual projections, in the diencephalon and mesencephalon, several days earlier. Thus, the retinohypothalamic projection is the last primary visual pathway to develop in the chick embryo.

Animals↗

Functional organization of the cat's visual cortex after prenatal interruption of binocular interactions.

The functional consequences of interrupting in utero binocular interactions were studied by recording from single cells in area 17 of adult cats that had one eye removed at least 2 wk before birth. In these animals all cortical neurons could be driven by the remaining eye, and in tangential microelectrode penetrations, sequences of neurons containing a full 180-degree cycle of preferred orientations were encountered. Other response properties of cortical neurons in the prenatally enucleated animals were also normal with the notable exception that the dimensions of receptive fields were significantly smaller when compared with those of control animals. Our results indicate that orientation columns in the visual cortex can develop independently of ocular dominance columns, and they suggest that interruption of binocular interactions during prenatal development of the visual pathways may enhance the resolving power of the remaining eye.

Animals↗

[A preliminary study on development of human visual system in fetus by DiI-tracing].

OBJECTIVE: To reveal the morphological features and dynamic processes of the development of inter-connections in the retina, lateral geniculate nucleus (LGN), superior colliculus (SC) and visual cortex (VC) in human fetal life by using a fluorescent tracer, 1, 1'-dioctadecyl-3, 3, 3', 3'-tetramethylin-docarbocyanine perchlorate (DiI). METHODS: DiI was embedded into the optic tract, brachium of superior colliculus and subplate of visual cortex in fixed postmortem human tissues of 7 fetuses. The tissue was incubated at 37 degrees C for 4 to 10 weeks (ws). After DiI had satisfactorily diffused via axons of the visual system, the tissue was sectioned, mounted and observed under a confocal laser scanning microscope. RESULTS: In 12 week-fetus, retinogeniculate axon has already reached LGN, but there was no cellular lamination. After embedment, axons from retina arrived at SC, and the fibers were distributed along the dorsal part of the SC. At 12 and 22 ws, there were subplates under visual cortex. CONCLUSION: The retinogeniculate axon reaches LGN before 12 ws and forms cellular lamination after 12 ws. The axon from retina reaches SC before 12 ws. The subplate under visual cortex forms before 12 ws and disappears after 22 ws. DiI can be easily and effectively used to label the axon of visual system of human fetus to study the prenatal development of human visual pathway.

Axons↗

Parallel pathways in the retina of Old and New World primates.

Old-world simians are all trichromats, but in most new-world primates there is a polymorphism; males are dichromats but most females are trichromats. In the old world simian, luminance and red-green chromatic channels defined by psychophysical experiments have as a basis parasol ganglion cells of the magnocellular (MC) pathway and midget ganglion cells of the parvocellular (PC) pathway respectively. Small bistratified ganglion cells provide a basis for a blue-yellow chromatic channel, which should probably be considered a separate entity. In both dichromatic and trichromatic new-world animals, the MC pathway and the small bistratified, blue-yellow system seem anatomically and physiologically similar to those in their old-world relatives. The midget ganglion cells of the parvocellular pathway in trichromats are anatomically and physiologically similar to the old-world pattern. In dichromatic animals, they are anatomically similar and physiologically resemble those of trichromatic animals, except for the lack of chromatic opponency. We conclude that these three systems may from a basic pattern for the visual pathway of primates. However, the results from dichromats indicate that the evolution of trichromacy may be found to be more complex than presently supposed.

Animals↗

Axonin 1 is expressed primarily in subclasses of avian sensory neurons during outgrowth.

A 120 kDa protein, which is expressed mainly on the surface of chick sensory neurons during outgrowth, was identified by monoclonal antibody 1A12. Crossreactivity studies showed that this protein was identical to axonin 1, a member of the immunoglobulin superfamily which promotes neurite outgrowth. Using the 1A12 antibody, we show that in the peripheral nervous system of the chick, axonin 1 is present on the cell bodies and processes of cutaneous and visceral neurons, but not on muscle afferents. In the central nervous system, axonin 1 is present in sensory pathways, such as fibers of the dorsal funiculi in the spinal cord and the optic pathway. However, axonin 1 is only expressed on growing nerve fibers. Late in embryonic development, it is present only on a small population of dorsal root ganglion cells, and is entirely absent on optic fibers. The disappearance of axonin 1 in the visual pathway coincides with the arrival of optic axons at the tectum, suggesting its expression is down regulated by axonal contact with its target. The localization of this protein on the surface of neuronal membranes was confirmed by EM immunohistochemistry and by labeling live nerve cells and their processes in tissue culture. The restricted spatio-temporal expression of axonin 1, together with its expression on the surface of neuronal membranes suggests that it is important for the development of sensory projections.

Animals↗

Retinotopy of the human retinal nerve fibre layer and optic nerve head.

The organisation of the primate nerve fibre layer and optic nerve head with respect to eccentricity or the positioning of central and peripheral axons remains controversial. Crystals of the carbocyanine dyes DiI (1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate), or DiA (4-[4-didecylaminostryryl]-N-methylpridiniumiodide) were used to trace retinal ganglion cell axons within the nerve fibre layer, optic nerve head, and optic nerve. The present study demonstrated that peripheral retinal axons were scattered throughout the vitreal-scleral depth of the nerve fibre layer. This scattered distribution was maintained as the fibres passed through the optic nerve head and into the optic nerve. Axons of the arcuate bundles showed a bias towards the scleral portions of the nerve fibre layer and a variable degree of fibre scatter across the nerve fibre layer which was not as evident in labelling from other retinal regions. There was a rough topographic representation within the optic nerve head according to retinal circumference such that both peripheral and central fibres were mixed within a wedge extending from the periphery to the centre of the nerve. Foveal fibres occupied a large proportion of the temporal aspect of the optic nerve head and nerve, whereas fibres from areas temporal to the fovea appeared to be displaced to more superior and inferior regions. Consistent with the scleral bias seen in the retina, arcuate fibres maintained a peripheral position as they passed through the optic nerve head and occupied a more peripheral position in the nerve. The present results suggest that any degree of order present within the optic nerve is not an active process; optic axons are not instructed to establish a retinotopic order within the initial portions of the visual pathway.

Adult↗

Inferior cortical altitudinal hemianopia: report of a case.

A case of bilateral inferior altitudinal hemianopia of cortical origin is reported. Although bilateral altitudinal hemianopias can be caused by more or less symmetrical involvement of visual pathways, it is shown how only three sites of these pathways are likely to be responsible for altitudinal hemianopias in human pathology.

Cerebrovascular Disorders↗

The maturation of form and motion perception in school age children.

The purpose of the current study was to investigate the maturation of form and motion perception, specifically the component visual abilities involved in the identification of motion-defined form, in children ranging in age from 3 to 12 years. Experiment 1 compared the maturation of motion-defined and texture-defined shape identification. Minimum speed thresholds on the motion-defined shape task decreased until age 7 years. Orientation difference thresholds on the texture-defined shape task decreased until age 11 years. Experiment 2 compared the maturation of global motion and global texture direction discrimination. Coherence thresholds on both tasks were similar in children of all ages and adults. Experiment 3 compared the maturation of direction discrimination on motion coherence and motion displacement tasks. Maximum displacement thresholds (Dmax) increased until age 7 years. The results are discussed with respect to the maturation of M/dorsal and P/ventral visual pathways.

Aging↗

Stereoscopic vision: solving the correspondence problem.

Neurons in early visual areas respond to horizontal disparity in images that do not give rise to stereopsis. False binocular matches, however, are discarded at the apex of the visual pathway: the activity of neurons in the primate inferior temporal cortex correlates directly with conscious depth perception.

Animals↗