Audie G. Leventhal

Degradation of stimulus selectivity of visual cortical cells in senescent rhesus monkeys

Human visual function declines with age. Much of this decline is probably mediated by changes in the central visual pathways. We compared the stimulus selectivity of cells in primary visual cortex (striate cortex or V1) in young adult and very old macaque monkeys using single-neuron in vivo electrophysiology. Our results provide evidence for a significant degradation of orientation and direction selectivity in senescent animals. The decreased selectivity of cells in old animals was accompanied by increased responsiveness to all orientations and directions as well as an increase in spontaneous activity. The decreased selectivities and increased excitability of cells in old animals are consistent with an age-related degeneration of intracortical inhibition. The neural changes described here could underlie declines in visual function during senescence.

Functional degradation of visual cortical cells in old cats.

Visual function declines with age. Using extracellular single-unit in vivo recordings, we compared the function of primary visual cortical (area 17) cells in young and old paralyzed, anesthetized cats. The results reveal that cortical neurons in old cats exhibit higher visually evoked responses, higher spontaneous activities, lower signal-to-noise ratios, and weaker orientation and direction selectivity than do cells in young adult cats. These findings are consistent with previously reported age related declines in cortical function in senescent macaque monkeys. Thus, similar declines in cortical function accompany old age in different mammalian species with well developed cortices.

Neural correlates of boundary perception

The responses of neurons in areas V1 (17) and V2 (18) of anesthetized and paralyzed rhesus monkeys and cats were recorded while presenting a set of computer-generated visual stimuli that varied in pattern, texture, luminance, and contrast. We find that a class of extrastriate cortical cells in cats and monkeys can signal the presence of boundaries regardless of the cue or cues that define the boundaries. These cue-invariant (CI) cells were rare in area V1 but easily found in V2. CI cortical cells responded more strongly to more salient boundaries regardless of the cue defining the boundaries. Many CI cortical cells responded to illusory contours and exhibited the same degree of orientation and direction selectivity when tested with boundaries defined by different cues. These cells have significant computational power inherent in their receptive fields since they were able to generalize across stimuli and integrate multiple cues simultaneously in order to signal boundaries. Cells in higher order cortical areas such as MT (Albright, 1992), MST (Geesaman & Anderson, 1996), and IT (Sary et al., 1993) have previously been reported to respond in a cue invariant fashion. The present results suggest that the ability to respond to boundaries in a cue-invariant manner originates at relatively early stages of cortical processing.

Functional degradation of extrastriate visual cortex in senescent rhesus monkeys

The receptive field properties of striate cortical (V1) cells degrade in senescent macaque monkeys. We have now carried out extracellular single unit studies of the receptive field properties of cells in extrastriate visual cortex (area V2) in very old rhesus (Macaca mulatta) monkeys. This study provides evidence that both the orientation and direction selectivities of V2 cells in old monkeys degrade significantly. Decreased selectivity is accompanied by increased visually driven and spontaneous responses. As a result, V2 cells in old animals exhibit markedly decreased signal-to-noise ratios. A significant degradation of neural function in extrastriate cortex may underlie the declines in higher order visual function that accompany normal aging.

Aging affects the direction selectivity of MT cells in rhesus monkeys

The ability to accurately perceive the direction and speed of moving objects declines during normal aging. This is likely due to functional degradation of cortical neurons. Most neurons in the primate middle temporal area (MT) are direction-selective and their activity is closely linked to the perception of coherent motion. We investigated the mechanisms that underlie this age-related decline by comparing the proportions of direction-selective MT cells in old and young macaque monkeys, using in vivo single-cell recording techniques. Our results showed that the proportion of such cells was lower in old than in young monkeys. Moreover, one type of direction-sensitive cells, pattern cells, was especially sensitive to aging and was affected more severely than another class, component cells. We also found that direction selectivity was affected more severely in MT than in V1 of senescent monkeys. Thus, the functional degradation of MT and V1 cells may mediate perceptual decline in visual motion tasks in old primates.

Aging affects contrast response functions and adaptation of middle temporal visual area neurons in rhesus monkeys

In the present study we studied the effects of aging on the coding of contrast in area V1 (primary visual cortex) and MT (middle temporal visual area) of the macaque monkey using single-neuron in vivo electrophysiology. Our results show that both MT and V1 neurons in old monkeys are less sensitive to contrast than those in young monkeys. Generally, contrast sensitivity is affected by aging more severely in MT cells than in V1 cells. Specifically, MT cells were affected more severely than motion direction selective V1 cells. Particularly, we found that MT neurons in old monkeys exhibited enhanced maximum visual responses, higher levels of spontaneous activity and decreased signal-to-noise ratios. In addition, we also found age-related changes in neuronal adaptation to visual motion in MT. Compared with young animals, the contrast gain of MT neurons in old monkeys is less affected, but the response gain by adaptation of MT neurons is more affected. Our results suggest that there may be an anomalous visual processing in both the magnocellular and parvocellular pathways. The neural changes described here are consistent with an age-related degeneration of intracortical inhibition and could underlie some deficits in visual function during normal aging.

Retinal ganglion cell dendritic fields in old-world monkeys are oriented radially

We analyzed the dendritic field morphology of 297 ganglion cells from peripheral regions of monkey retina. Most of the dendritic fields were elongated, and there was a significant tendency for the dendritic fields to be oriented radially, i.e., like the spokes of a wheel with the fovea at the hub. An overrepresentation of radial orientations in the peripheral retina of primates might explain why humans are best able to detect stimuli which are oriented radially using peripheral vision.

Aging Affects the Neural Representation of Speed in Macaque Area MT

Human perception of speed declines with age. Much of the decline is probably mediated by changes in the middle temporal (MT) area, an extrastriate area whose neural activity is linked to the perception of speed. In the present study, we used random-dot patterns to study the effects of aging on speed-tuning curves in cortical area MT of macaque visual cortex. Our results provide evidence for a significant degradation of speed selectivity in MT. Cells in old animals preferred lower speeds than did those in young animals. Response modulation and discriminative capacity for speed in old monkeys were also significantly weaker than those in young ones. Concurrently, MT cells in old monkeys showed increased baseline responses, peak responses and response variability, and these changes were accompanied by decreased signal-to-noise ratios. We also found that speed discrimination thresholds in old animals were higher than in young ones. The foregoing neural changes may mediate the declines in visual motion perception that occur during senescence.

Spatial and temporal sensitivity degradation of primary visual cortical cells in senescent rhesus monkeys

Human visual function declines with age. Much of this decline is mediated by changes in the central visual pathways. In this study we compared the spatial and temporal sensitivities of striate cortical cells in young and old paralysed macaque monkeys. Extracellular single‐unit recordings were employed. Our results show that cortical neurons in old monkeys exhibit lower optimal spatial and temporal frequencies, lower spatial resolution and lower high temporal frequency cut‐offs than do cells in young adult monkeys. These changes in old monkeys are accompanied by increased visually evoked responses, increased spontaneous activities and decreased signal‐to‐noise ratios. The increased excitability of cells in old animals is consistent with an age‐related degeneration of intracortical inhibition. The degradation of spatial and temporal function in old striate cortex should contribute to the decline in visual function that accompanies normal aging.

Stimulus dependence of orientation and direction sensitivity of cat LGNd relay cells without cortical inputs: A comparison with area 17 cells

The cortical contribution to the orientation and direction sensitivity of LGNd relay cells was investigated by recording the responses of relay cells to drifting sinusoidal gratings of varying spatial frequencies, moving bars, and moving spots in cats in which the visual cortex (areas 17, 18, 19, and LS) was ablated. For comparison, the spatial-frequency dependence of orientation and direction tuning of striate cortical cells was investigated employing the same quantitative techniques used to test LGNd cells. There are no significant differences in the orientation and direction tuning to relay cells in the LGNd of normal and decorticate cats. The orientation and direction sensitivities of cortical cells are dependent on stimulus parameters in a fashion qualitatively similar to that of LGNd cells. The differences in the spatial-frequency bandwidths of LGNd cells and cortical cells may explain many of their differences in orientation and direction tuning. Although factors beyond narrowness of spatial-frequency tuning must exist to account for the much stronger orientation and direction preferences of cells in area 17 when compared to LGNd cells, the evidence suggests that the orientation and direction biases present in the afferents to the visual cortex may contribute to the orientation and direction selectivities found in cortical cells.