Peter D. Spear

Neural bases of visual deficits during aging

Visual abilities decline during normal (non-pathological) aging. Many of these visual declines cannot be attributed to optical changes and must therefore be due to changes in the retina or central visual pathways. These include declines in visual acuity and spatial contrast sensitivity (especially under low luminance levels), suprathreshold contrast vision and contrast gain, temporal-frequency contrast sensitivity and resolution, spatial-temporal interactions, hyperacuity, binocular processing, and sensitivity to motion. Certain aspects of these vision deficits and comparisons with neurophysiological and lesion-behavior studies in monkeys suggest hypotheses about the nature and location (e.g. magnocellular vs parvocellular pathways, specific visual structures, and so on) of the neural deficits. Despite the well-documented psychophysical deficits, available anatomical studies in humans and monkeys suggest that aging has only relatively minor effects on the retino-geniculo-striate pathway. Retinal photoreceptor losses are relatively restricted to rods, and there is compensation among the remaining rods for those that are lost. Although some retinal ganglion cells appear to be lost, the loss is small relative to individual-to-individual variability. In addition, there appear to be no massive cell losses in the LGN or striate cortex. Physiological results in the monkey LGN suggest that the functional properties of LGN neurons, and therefore their retinal inputs, are not significantly affected by aging. Retinal pattern-evoked ERG studies in humans likewise suggest that the physiological properties of the retina are little affected by aging. Comparisons between pattern-evoked ERG and cortical evoked potentials in the same individuals suggest that some neural change occurs between the retina and striate cortex, but the location and nature of this change is not known. Thus, we are far from being able to answer the question, What are the neural bases of visual deficits during aging? There are several possible reasons for this: (1) The neurobiological methods that have been brought to bear on the question have been fairly limited. (2) Investigations of neural changes may not have been guided sufficiently by what is known about the psychophysical changes that occur with aging. (3) Existing studies may not have examined the correct locations in the visual system. (4) There is large individual-to-individual variability in the effects of aging and, with the small samples of individuals that typically are available in neural studies of aging, the variability could obscure detection of aging-related changes. Suggestions are offered for ways in which future research can solve these problems.(ABSTRACT TRUNCATED AT 400 WORDS)

Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons

The influence of the cortico-geniculate pathway on identified X and Y lateral geniculate cells was studied by reversibly cooling visual cortical areas 17 and 18. The majority (86.5%) of cells changed their response to visual stimulation when cortex was inactivated, and both X- and Y-cells were modulated by the cortical input. The influence of the visual cortex was complex, with both excitatory and inhibitory actions. Furthermore, the mechanism underlying the basic center-surround receptive field organization was influenced.

Effects of aging on the densities, numbers, and sizes of retinal ganglion cells in rhesus monkey

We used sterological procedures that yield unbiased estimates to quantify the densities, numbers, and soma sizes of retinal ganglion cells in seven young adult and six old rhesus monkeys. The retinae were flat mounted so that we could determine whether there are different aging-related losses in different retinal regions. The mean (+/-standard deviation) total number of ganglion cells was 1,529,039 +/- 115,260 in young-adult retinae and 1,556,698 +/- 165,056 in old retinae, a difference that was not statistically significant. There also were no significant differences between young and old retinae in the densities or total numbers of ganglion cells in the four retinal quadrants, in four concentric retinal zones from fovea to peripheral retina, or in smaller hemiretinal regions of the concentric zones. Ganglion-cell soma sizes also did not differ significantly between young and old animals. Moreover, counts of the largest ganglion cells, which probably correspond to P alpha ganglion cells, revealed no selective loss of these cells with aging. These results are consistent with our previous anatomical and physiological studies of the LGN. Together they suggest that the retino-geniculate pathways are relatively unaffected by aging in the rhesus monkey.

How complete is physiological compensation in extrastriate cortex after visual cortex damage in kittens

SummaryPrevious studies indicate that neurons in the cats posteromedial lateral suprasylvian (PMLS) visual area of cortex show physiological compensation after neonatal but not adult damage to areas 17, 18, and 19 of the visual cortex (collectively, VC). Thus, VC damage in adults produces a loss of direction selectivity and a decrease in response to the ipsilateral eye among PMLS cells, but these changes are not seen in adult cats that received VC damage as kittens. This represents compensation for early VC damage in the sense that PMLS neurons develop properties they would have had if there had been no brain damage. However, this is only a partial compensation for the effects of VC damage. A full compensation would involve development of properties of the VC cells that were removed in the damage. The present study investigated whether this type of compensation occurs for detailed spatial- and temporal-frequency processing. Single-cell recordings were made in PMLS cortex of adult cats that had received a VC lesion on the day of birth or at 8 weeks of age. Responses to sine-wave gratings that varied in spatial frequency, contrast, and temporal frequency were assessed quantitatively. We found that the spatial- and temporal-frequency processing of PMLS cells in adult cats that had neonatal VC damage were not significantly different from PMLS cells in normal cats. Therefore, there was no evidence that PMLS cells can compensate for VC damage by developing properties that are better than normal and like those of the striate cortex cells that were damaged.We also assessed the effects of long-term VC damage in adult cats to determine whether the normal properties seen in cats with neonatal VC damage represent a compensation for abnormalities in PMLS cortex present after adult damage. In a previous study, we found that acute VC damage in adult cats has small but reliable effects on maximal response amplitude, maximal contrast sensitivity, and spatial resolution (Guido et al. 1990b). In the present study, we found that long-term VC damage in adult cats does not increase these abnormalities as a result of secondary degenerative changes. In fact, the minor abnormalities that were present after an acute VC lesion were virtually absent following a long-term adult lesion, perhaps because they were due to transient traumatic effects. Therefore, there was little evidence for abnormalities in spatial- or temporal-frequency processing following long-term adult VC damage for which PMLS cells might show compensation following long-term neonatal damage.Our results thus indicate that there is little or no difference in the spatial- or temporal-frequency processing of PMLS cells in normal cats and cats with long-term VC damage received early in life or as adults. These findings are discussed in relation to the inputs to PMLS cortex and to the behavioral abilities of cats with VC damage at different ages. The implications for under-standing the role of lateral suprasylvian visual cortex in behavioral recovery from VC damage is considered.

Effects of aging on numbers and sizes of neurons in histochemically defined subregions of monkey striate cortex.

In addition to its horizontal layers, primate striate cortex has a vertical modular organization. Among the vertical modules are histochemically defined areas of high and low cytochrome oxidase labeling in the supragranular layers, referred to, respectively, as blobs and interblobs. Cytochrome c oxidase (CO) blobs and interblobs differ in their inputs from the magnocellular and parvocellular visual pathways, their physiological properties, and many aspects of their neurochemistry. The present study investigated whether aging differentially affects neuron numbers or sizes in the supragranular blobs or interblobs.

Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens

SummaryPrevious studies have shown that functional compensation is present in the cats posteromedial lateral suprasylvian (PMLS) area of cortex after damage to areas 17, 18, and 19 (visual cortex) early in life but not after damage in adults. These studies all have investigated animals with a unilateral visual cortex lesion, whereas all behavioral studies of compensation for early visual cortex damage have investigated animals with a bilateral lesion. In the present experiment, we investigated whether functional compensation also is present in PMLS cortex after a bilateral visual cortex lesion early in life. We recorded from single neurons in the PMLS cortex of adult cats that had received a bilateral lesion of areas 17, 18, and 19 on the day of birth or at 8 weeks of age. We found that PMLS cells in both groups of cats had functional compensation (normal direction selectivity and ocular dominance) similar to that seen after a unilateral lesion at the same ages. These results are consistent with the hypothesis that PMLS cortex is involved in the behavioral compensation seen after early visual cortex damage. In addition, the results indicate that inputs from contralateral visual cortex are not necessary for the development of functional compensation seen in PMLS cortex.

Critical period for the marked loss of retinal X-cells following visual cortex damage in cats

Visual cortex damage in newborn kittens produces a 78% loss of retinal X-cells whereas damage in adult cats produces only a 22% loss. Retinal Y- and W-cells are unaffected. The present experiment showed that the critical period for the severe loss of retinal X-cells ends between birth and 2 weeks of age. These results have implications for understanding the neural mechanisms of recovery from early visual cortex damage.

Neurophysiological mechanisms of recovery from visual cortex damage in cats: Properties of lateral suprasylvian visual area neurons following behavioral recovery

SummaryDamage to visual cortical areas 17, 18, and 19 in the cat produces severe and long-lasting deficits in performance of form and pattern discriminations. However, with extensive retraining the animals are able to recover their ability to discriminate form and pattern stimuli. Recent behavioral experiments from this laboratory have shown that a nearby region of cortex, the lateral suprasylvian visual area (LS area), plays an important role in this recovery (Wood et al., 1974; Baumann and Spear, 1977b). The present experiment investigated the underlying neurophysiological mechanisms of the recovery by recording from single neurons in the LS area of cats which had recovered from long-term visual cortex damage.Five adult cats received bilateral removal of areas 17, 18, and 19. They were then trained to criterion on two-choice brightness, form, and pattern discriminations. Recording from LS area neurons was carried out after the behavioral training, from 3 to 7 months after the visual cortex lesions. The properties of these neurons were compared to those of LS area neurons in normal cats (Spear and Baumann, 1975) and in cats with acute or short-term visual cortex damage and no behavioral recovery (Spear and Baumann, 1979). The results showed that all of the changes from normal which were produced by acute visual cortex damage were also present after the behavioral recovery. Moreover, all of the response properties of LS area neurons which remain after acute visual cortex damage were present in similar form after the behavioral recovery. There was no evidence for any functional reorganization in the LS area concomitant with its role in the behavioral recovery.These results suggest that functional reorganization plays little or no role in recovery from visual cortex damage in adult cats. Rather, the recovery of form and pattern discrimination ability appears to be based upon the functioning of residual neural processes in the LS area which remain after the visual cortex damage.

Effects of lateral suprasylvian visual cortex lesions on visual localization, discrimination, and attention in cats

Experiments were carried out to begin to define the behavioral functions of the lateral suprasylvian (LS) visual area of the cats cortex. Behavioral tasks were chosen for analysis on the basis of previous suggestions in the literature concerning possible functions of LS cortex and its afferent pathways. These tasks included the ability of cats to orient the head and eyes to a stimulus presented in particular locations in the visual field, the ability to learn successive reversals of a two-choice visual pattern discrimination, and the ability to maintain or shift attention between relevant or irrelevant visual form and brightness cues. Eight cats were trained on each of these tasks. Four of the cats then received bilateral lesions of LS cortex, including the AMLS and PMLS regions, and the remaining 4 cats were used to assess normal retention. The LS cortex lesions had no significant effect upon performance of any of the behaviors tested. Thus, this region of cortex appears to play no essential role in simple brightness, form, and pattern discrimination performance, visual reversal learning, maintaining and shifting visual attention, or orienting the head and eyes to stimuli in the visual field. These results are discussed in relation to previous lesion studies involving large regions of the cats extrastriate cortex and studies in other species. Possible functions of LS cortex, based upon recent electrophysiological studies, are suggested.

Functional influence of areas 17, 18, and 19 on lateral suprasylvian cortex in kittens and adult cats: implications for compensation following early visual cortex damage

The aim of the present study was to investigate the mechanisms of physiological compensation that is seen in the posteromedial lateral suprasylvian (PMLS) cortex of cats that received visual cortex (areas 17, 18, and 19) damage early in life. The strategy was to compare the response properties of PMLS neurons just after visual cortex damage (before any compensation has occurred) with the properties of PMLS neurons in normal cats and cats with long-standing visual cortex damage. Fourteen animals (aged 8 weeks, 18 weeks, 26 weeks, or adult) received a unilateral visual cortex lesion and recordings were made from ipsilateral PMLS cortex within about 24 h. An additional 4 adult cats were studied within either 24 or 3 h of a bilateral visual cortex lesion. Results from these animals were compared with results from normal cats and cats with long-standing visual cortex damage studied previously in this laboratory. At all ages studied, an acute visual cortex lesion reduced the percentage of direction-sensitive cells in PMLS cortex from nearly 80% in normal cats to about 20% after the lesion. In 8- and 18-week-old kittens, nearly all of the remaining PMLS cells responded best to stimulus movement but were not direction sensitive. In 26-week-old and adult cats, the remaining cells were divided between those that responded to movement without a directional preference and those that responded as well to stationary flashed stimuli as to moving stimuli. The presence of receptive-field surround inhibition was not affected significantly by an acute lesion at any age. In addition, few PMLS cells were orientation selective to elongated slits of light in cats with an acute lesion, just as in normal cats. The ocular dominance distributions of PMLS neurons also were normal following an acute visual cortex lesion at all ages studied. These results suggest that the influences of areas 17, 18, and 19 on the response properties of PMLS neurons are the same when the properties first reach maturity as in adult cats. The results also suggest that the mechanisms of physiological compensation for an early visual cortex lesion differ for different response properties. Compensation of direction sensitivity and orientation selectivity (an anomalous property) develops de novo after the early lesion. In contrast, compensation of ocular dominance appears to be due to the maintenance of a preexisting property that is present immediately after the lesion. Thus, plasticity after early visual cortex damage represents multiple developmental changes in the remaining visual pathways.