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Effects of aging on the primate visual system: spatial and temporal processing by lateral geniculate neurons in young adult and old rhesus monkeys.

1. Visual abilities decline during normal aging, and many of these declines are due to neural changes in the retina or central visual pathways. We have begun studies of the primate visual system to investigate the location and nature of these changes as well as to answer general questions about the effects of aging on neural function. We began with the dorsal lateral geniculate nucleus (LGN) because it is the main structure through which visual information passes on the way to cortex and because the parallel parvocellular and magnocellular pathways, which may be affected differently by aging, are anatomically distinct there. 2. Single-cell recordings were made in the LGN of young adult (5-16 yr) and old (25-28 yr) rhesus monkeys. We made quantitative measures of a wide variety of response properties for a large number of parvocellular (n = 257) and magnocellular (n = 113) neurons in the two groups of animals. As a result, in addition to studying the effects of aging, we were able to make quantitative comparisons between parvocellular and magnocellular neurons using larger samples than have been studied previously and for some properties that have not been studied before. 3. We found that magnocellular neurons have significantly higher maximal response rates and signal-to-noise ratios than parvocellular neurons. However, response latencies to visual stimulation were similar for neurons in the two types of layers. In agreement with previous studies, magnocellular neurons had higher maximal contrast sensitivity and higher contrast gain than parvocellular neurons. However, the sensitivity difference occurred because nearly all of the neurons with low sensitivities (< 10) were in the parvocellular layers, not because neurons in the magnocellular layers had the highest sensitivities. 4. Neurons with the smallest receptive-field centers, the highest spatial-frequency resolutions, and the highest optimal spatial frequencies were found in the parvocellular layers. However, the overall distributions of each of these properties overlapped substantially for neurons in the two types of layers, and the mean values were not significantly different. The mean high temporal-frequency cutoff was significantly higher for magnocellular than parvocellular neurons, but the difference was small (only 3 Hz), and it occurred because many parvocellular neurons had lower cutoffs than any seen in the magnocellular layers, not because magnocellular neurons had the highest temporal-frequency cutoffs. Parvocellular neurons also had narrower temporal-frequency tuning than magnocellular neurons. However, there was no significant difference in optimal temporal frequency.(ABSTRACT TRUNCATED AT 400 WORDS)

Aging↗

[Activation response to photic stimulation in normal cats and after transection of the afferent pathways of the mesencephalic reticular formation].

In chronic experiments on waking unrestrained cats with implanted electrodes the reaction of EEG activation to light stimulation was recorded in two sets of experiments in normal cats and in animals with transsection of brachia colliculi superioris that separated mesencephalic reticular system. The intensity of the activating reaction in the intact cats increased ith a rise in the light stimulus intensity. In the cats with brachia-colliculi superioris transsected there was no definite dependence on the stimuli intensity and the intensity of the activating reaction changed randomly. It is suggested that this irregularity is accounted for by blocking of the excitating afferent flow usually coming to the mesencephalic reticular formation through brachia and colliculi both from the visual pathways (ascending flow) and from the cortex (descending activation regulating flow).

Animals↗

Normal planum temporale asymmetry in dyslexics with a magnocellular pathway deficit.

Developmental dyslexia has been associated with both abnormal hemispheric symmetry of the planum temporale (PT) and a deficit in the magnocellular visual pathway. We examined the relationship between these two abnormalities. Using sagittal magnetic resonance images and three methods, we measured the PT in dyslexic subjects with a documented magnocellular deficit and controls. Dyslexic subjects did not deviate from normal leftward PT asymmetry, but both groups became less left-lateralized with methods that excluded sulcul tissue. Results suggest that dyslexic subjects with a magnocellular deficit do not always have abnormal symmetry of the PT. PT symmetry may instead be related to a different subtype of dyslexia. In addition, PT asymmetry in any subject group depends on the measurement method.

Adult↗

Non-arteritic anterior ischaemic optic neuropathy: evaluation of the brain and optic pathway by conventional MRI and magnetisation transfer imaging.

The purpose of the study was to examine the brain and the visual pathway of patients with non-arteritic anterior ischaemic optic neuropathy (NAION) by using conventional MRI (cMRI) and volumetric magnetisation transfer imaging (MTI). Thirty NAION patients, aged 67.5 +/- 8.14 years, and 28 age- and gender-matched controls were studied. MTI was used to measure the magnetisation transfer ratio (MTR) of the chiasm and for MTR histograms of the brain. The presence of areas of white matter hyperintensity (WMH) was evaluated on fluid-attenuated inversion recovery (FLAIR) images. Area of the optic nerves (ONs) and volume of the chiasm were assessed, as were coronal short-tau inversion recovery (STIR) and MTI images, respectively. More areas of WMH were observed in patients (total 419; mean 14.4; SD 19) than in controls (total 127; mean 4.7; SD 5.7), P < 0.001. Area (in square millimetres) of the affected ONs, volume(in cubic millimetres) and MTR (in percent) of the chiasm (10.7 +/- 4.6), (75.8 +/- 20.2), (56.4 +/- 6.5), respectively, were lower in patients than in controls (13.6 +/- 4.3), (158.2 +/- 75.3) (62.1 +/- 6.2), respectively, P < 0.05. Mean MTR of brain histograms was lower in patients (53.0 +/- 8.0) than in controls (58.0 +/- 5.6), P < 0.05. NAION is characterised by decreased ON and chiasmatic size. The low MTR of the chiasm and brain associated with increased areas of WMH may be suggestive of demyelination and axonal damage due to generalised cerebral vascular disease.

Aged↗

L-[3H]lysine binding to rat retinal membrane: I. Quantitative determination and characterization of the binding sites.

A saturable reversible binding to membranes from rat retina has been found for L-[3H]lysine. Specific binding is time, temperature and protein concentration-dependent, and shows stereospecificity. The best computer fits of the experimental data are obtained with a receptor model based on two independent binding sites, of which only one site with a Kd value of 229.4 +/- 14.23 nM and a Bmax of 2.04 +/- 0.11 pmol/mg protein could be characterized satisfactorily. Several compounds included putative neurotransmitters have moderate or no affinity for L-lysine binding sites. A different pattern of distribution of L-[3H]lysine binding sites is observed among various regions of the brain, with the highest density in the occipital cortex, and the lowest density in ponsmedulla. The existence of binding sites in rat retinal membranes for L-lysine, as well as in the areas involved in the visual pathway, suggests a role for this amino acid in the physiological mechanism of the visual function.

Animals↗

Optic neuritis. Differential losses of luminance and chromatic function near a scotoma.

Visual sensitivity to achromatic and chromatic stimulus flashes was determined at sites just inside, on the boundary and just outside scotomata in 11 patients with recovered optic neuritis. The colour of the flashes and the size of the steady background on which they appeared were such that detection was more likely to be mediated by either the large-diameter, magnocellular fibres or the small-diameter, parvocellular fibres of the anterior visual pathway. The spacing of the test sites ranged from 0.5 degrees to 4 degrees visual angle, depending on the shape and location of the scotomata. The greatest differences in sensitivity were between sites just inside and just outside the scotoma and in response to achromatic stimuli more likely to involve the magnocellular fibres. This effect may be due to the size of magnocellular fibres or to their relatively smaller numbers.

Adult↗

Functional MRI of self-controlled stereoscopic depth perception.

Stereoscopic depth perception was studied in healthy young adults using fMRI imaging at 2.0 T. In a novel paradigm we compared the cortical activation elicited by single-image stereograms which create alternating 2D and 3D percepts (event-related analysis triggered on the self-controlled switches between the two percepts) with the activation caused by a more conventional approach contrasting pairs of stereoscopic images with pairs of identical images (block design). The data show a distributed network of cortical areas embedded within the visual pathways that included about one-quarter of the cortical surface activated by 2D visual stimulation and about one-half of the area activated by 3D percepts based on stereoscopic image pair. 3D perception recruited mostly neuronal populations in higher order visual areas: whereas about 40% of the visually activated locations along the intraparietal sulcus were also activated by 3D perception based on single-image stereograms (resp. 90% stereoscopic images), only 10% such overlap was found in striate cortex. The study revealed no sup-port for a right-hemispheric lateralization of depth perception.

Adult↗

Electrophysiological evidence for a bisynaptic retinocerebellar pathway.

1. Electrical microstimulation was applied to an in vitro turtle brain preparation while recording extracellular activity from the cerebellar cortex. A visual input to the cerebellum was investigated by measuring spike responses evoked by stimulation of drifting visual patterns imaged onto the contralateral retinal eyecup. A vestibular input was assessed by extracellular field potentials following brief current pulses through monopolar suction electrodes holding the eighth cranial nerve (nVIII). 2. The cortical topography of visual and vestibular inputs was first examined. Visual units and vestibular fields show considerable topographic overlap in the rostrolateral quadrant of the cerebellum. In addition, granule layer units were isolated that responded to current stimulation of nVIII (60-150 microA monopolar). In some cases, spikes occurred at short and fixed latency after each current pulse for stimulus frequencies of 100 Hz. The responses of these units suggest a direct path between the stimulating and recording electrodes without intervening synapses. Alternatively, extracellular units were also encountered that responded with longer, more variable latencies but only for low stimulation frequencies (< or = 20 Hz). Of the units that responded to nVIII stimulation, three units also responded to visual stimuli, yet those units all failed to follow high-frequency stimulation of nVIII. This cortical area may then be a site for convergence of visual and vestibular signals on postsynaptic cells. 3. The cellular identity of the visual units in the granule layer and the visual pathways leading there were next investigated.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Characteristics of neurones projecting from the supraoesophageal ganglion in the shadow reflex pathway of the barnacle.

Barnacles respond to decreases in light intensity (shadows). Previous evidence indicates that the first stages of the visual pathway within the supraoesophageal ganglion comprise a limited number of neurones: a single pair of second-order neurones (I-cells), a pair of third-order projection neurones (A-cells), and at least five other projection neurones (four A-like shadow-excited cells and one shadow-inhibited cell) whose spikes may be recorded extracellularly from the circum-oesophageal connective nerve. Here we present evidence that information in this pathway diverges at the A-cell stage. Destruction of both A-cells by intense illumination of cells injected with carboxyfluorescein abolishes all shadow-evoked activity in the connectives and also the ability of shadows to influence motor neurones in the ventral ganglion. In addition, we have located the somata of these previously unidentified projection neurones, injected them with carboxyfluorescein, and observed that they have distinct branching patterns different from that of the A-cell. We name these cells 'alpha' (alpha), 'beta' (beta) and 'gamma' (gamma) cells. Simultaneous impalements show that A-cells drive at least one of the beta-cells but not vice versa. The same observation has not yet been made with regard to alpha- or gamma-cells. Depolarizing an I-cell does not readily drive a beta-cell impaled simultaneously. These observations support our conclusion that information diverges from the A-cells and not from the second-order I-cells to the other projection neurones in this ganglion.

Action Potentials↗

Differential inhibition of chromatic and achromatic perception by transcranial magnetic stimulation of the human visual cortex.

The magnocellular visual pathway is devoted to low-contrast achromatic and motion perception whereas the parvocellular pathway deals with chromatic and high resolution spatial vision. To specifically separate perception mediated by these pathways we have used low-contrast Gaussian filtered black-white or coloured visual stimuli. By use of transcranial magnetic stimulation (TMS) over the visual cortex inhibition of magnocellular stimuli was achieved distinctly earlier by about 40 ms compared with parvocellular information. A nonspecific inhibition of all stimuli could be seen peaking at 75-90 ms, significantly higher for magnocellular stimuli. The particular vulnerability of magnocellular stimuli to TMS is correlated with distinct physiological properties of this pathway such as faster conduction velocity and non-linear stimulus encoding.

Analysis of Variance↗

Spatial organization of the pigeon tectorotundal pathway: an interdigitating topographic arrangement.

The retinotectofugal system is the main visual pathway projecting upon the telencephalon in birds and many other nonmammalian vertebrates. The ascending tectal projection arises exclusively from cells located in layer 13 of the optic tectum and is directed bilaterally toward the thalamic nucleus rotundus. Although previous studies provided evidence that different types of tectal layer 13 cells project to different subdivisions in Rt, apparently without maintaining a retinotopic organization, the detailed spatial organization of this projection remains obscure. We reexamined the pigeon tectorotundal projection using conventional tracing techniques plus a new method devised to perform small deep-brain microinjections of crystalline tracers. We found that discrete injections involving restricted zones within one subdivision retrogradely label a small fraction of layer 13 cells that are distributed throughout the layer, covering most of the tectal representation of the contralateral visual field. Double-tracer injections in one subdivision label distinct but intermingled sets of layer 13 neurons. These results, together with the tracing of tectal axonal terminal fields in the rotundus, lead us to propose a novel "interdigitating" topographic arrangement for the tectorotundal projection, in which intermingled sets of layer 13 cells, presumably of the same particular class and distributed in an organized fashion throughout the surface of the tectum, terminate in separate regions within one subdivision. This spatial organization has significant consequences for the understanding of the physiological and functional properties of the tectofugal pathway in birds.

Animals↗

Orthograde axonal and transcellular transport of different fluorescent tracers in the primary visual system of the rat.

The differential labeling properties of various fluorescent tracers injected intraocularly were investigated using as a model the rat primary visual system. All of the tracers tested (Fast Blue, FB; True Blue, TB; Nuclear Yellow, NY; bisbenzimide, BB; Evans Blue, EB; propidium iodide, PI) produced a retrograde neuronal labeling of oculomotor neurons. However, no such labeling was observed in the medial pretectal nucleus (NPM) considered to be the site of origin of the rat centrifugal visual pathway. Orthograde transport within the axons of the optic tract and their terminal arborizations were visualized directly with FB and TB. No evidence of EB or PI orthograde transport was demonstrated. Furthermore, FB, TB, NY and BB displayed varying degrees of leakage from the optic axons and terminals into the extracellular space, there to be taken up by glial (FB, TB, NY, BB) and neuronal (NY, BB) somas of the primary optic system or in adjacent structures including NPM (BB). The neuronal labeling with NY or BB does not result from the retrograde axonal transport but appears to involve an orthograde transneuronal process transport. Some limitations in the use of different fluorescent tracers for determining neuronal connections are discussed.

Animals↗

Abnormal visual projection in a human albino studied with functional magnetic resonance imaging and visual evoked potentials.

The albino visual pathway is abnormal in that many fibres from the temporal retina project to the contralateral visual cortex. The visual projections in a human albino and a control have been investigated with fMRI and VEP during independent visual stimulation of both hemifields. Activity in the occipital cortex in the normal was contralateral to the stimulated visual field, whereas it was contralateral to the stimulated eye in the albino, independent of the stimulated visual field. Thus, the albino visual cortex is activated not only by stimulation in the contralateral visual field, but also by abnormal input representing the ipsilateral visual field. These novel findings help elucidate the nature of albino misrouting.

Albinism, Oculocutaneous↗

Visual input to the visuomotor mechanisms of the monkey's parietal lobe.

A newly identified class of neurons of the parietal cortex, studied in waking monkeys (Macaca mulatta), is activated by visual stimuli, perhaps via the retino-collicular visual pathway. This afferent input is thought to provide the visual cues activating the visuomotor mechanisms of the parietal lobe for the direction of visual attention.

Action Potentials↗

Albinism.

Albinism is the term applied to a heterogeneous group of genetically determined disorders characterized by hypopigmentation and affecting the eyes. After describing the clinical features of albinism in general, the authors discuss the various forms of oculocutaneous albinism, ocular albinism, and albinoidism that are of interest to the ophthalmologist. Emphasis is placed on the ocular features of each form. The visual pathway abnormalities and the clinical management of albinism are discussed.

Albinism↗

Structural development of the lateral geniculate nucleus and visual cortex in monkey and man.

This study concerns the development of the primary visual pathway of the primate. The lateral geniculate nucleus (LGN) is the principal thalamic relay to the visual cortex (area 17), and its neurons have similar morphological characteristics in both monkey and man, as identified by Golgi impregnation. The commonest neuron is the multipolar with a radiate or tufted dendritic tree; next is the bipolar neuron with two or three diametrically opposed dendritic trunks. Less frequent are neurons with beaded dendrites and others with fine, axon-like dendritic processes, possibly interneurons. The dendritic tree of all neurons remains generally within a lamina, but some dendrites cross interlaminar zones. LGN neurons are identifiable before birth and differ from their adult form by the presence of immature features, especially numerous dendritic and somatic spines, most frequent at birth in monkeys and at about 4 months postnatally in man. They disappear almost completely by 3 months in monkeys and 9 months in man. The human LGN has reached its 'adult' volume by this age. Two stages in the development of the human area 17 can be defined. The first is marked by a rapid growth to its 'adult' volume by about 4 months, and by intense synaptogenesis beginning in the foetus and reaching a maximum around 8 months. The second stage is one of stabilization in the volume of area 17 and loss of synapses to reach 'adult' synaptic density around 11 years, at about 60% of the maximum values.

Adolescent↗

Cortical representation of visual three-dimensional space.

Perception of real depth includes information on stereopsis and distance. How both interact in the visual pathway was the subject of a study performed on the behaving monkey. Neurons in the primary visual cortex (area V1) have their activity, visual and/or spontaneous, modulated by the viewing distance. Disparity selectivity may be present or better expressed at a given viewing distance. This modulation is independent of the visual pattern. The use of prisms shows that vergence is implicated in this phenomenon. Consequently, extraretinal signals related to ocular motility have access to area V1. Among them, proprioceptive signals from the eye muscles have been shown to be involved in visual cortical function and in the development of depth perception. It is possible that the same signals may also be involved in the distance modulation shown in V1 neurons, but this remains to be examined. A possible specialisation of disparity-selective cells in different cortical areas is discussed.

Animals↗

A new class of visual defect. Spreading inhibition elicited by chromatic light stimuli.

This paper deals with a single male subject, M., who has a well-defined visual defect of a kind not previously described. The defect is associated with a potent inhibitory response to long-wavelength stimuli, which spreads for up to 12 deg from the area of stimulation, suppressing M.'s detection of other high contrast stimuli. The effect can also be observed, weakly, with certain other coloured stimuli, but not with yellows or whites. Detailed psychophysical data are given for threshold sensitivity, colour matching, two-colour increment thresholds and visual acuity, all of which are more or less abnormal, depending on the stimulus colour. No abnormal effects were, however, observed with white light stimuli. On the basis of M.'s ability to fuse red and green random dot stereogram pairs, we argue that the inhibition arises centrally in the visual pathways. and we examine the implications of M.'s response characteristics for the analysis of central visual processing.

Adult↗