Lillian Tong

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.

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.

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.

Developmentally induced loss of direction-selective neurons in the cat's lateral suprasylvian visual cortex

Single-cell recordings were carried out in the posteromedial lateral suprasylvian (PMLS) visual cortex of cats reared in an environment illuminated by 8-Hz stroboscopic flashes. These cats had a reduced proportion of direction-selective cells (8%) compared to PMLS cortex of normal cats (79%). Other receptive-field properties and ocular dominance of the neurons appeared normal. These results have implications for understanding the mechanisms of PMLS-cortex development and for interpreting behavioral studies of strobe-reared cats.

Development of neuronal responses in cat posteromedial lateral suprasylvian visual cortex.

We studied the normal development of responses to visual stimulation among neurons in the posteromedial lateral suprasylvian (PMLS) visual cortex, an extrastriate visual cortical area in cats. Recordings were made from 495 single neurons in 19 kittens that were 2, 3, 4, 8, or 12 weeks of age, and the results were compared with those from normal adult cats. The percentage of neurons that respond to light increased from 57% in 2-week-old kittens to approximately adult values in 8-week-old kittens (81%). The strength and consistency of neuronal responses also increased with age. Nearly all of the responsive cells had well-defined excitatory receptive-field centers, and the receptive-field center sizes were similar to adults at all ages studied. However, few cells (5%) had inhibitory receptive-field surrounds in 2-week-old kittens. The incidence of surround inhibition increased to adult levels (about 40% of the cells) by 8 weeks of age, and the strength of surround inhibition also increased with age. Most cells responded best to moving stimuli in 2-week-old kittens, just as in adults. However, only about 20% of the responsive cells were direction sensitive at 2 weeks of age. The percentage of direction-sensitive cells increased gradually with age and reached approximately adult values by 8 weeks of age (74%). Once cells developed complete direction selectivity, with no response in the null direction, directional tuning width was similar to that in adults. When tested with slits of light flashed at various orientations or with spots and slits moving in various directions, few cells (8% or less) showed orientation selectivity at any age, just as in adults. Most of the cells were binocularly driven, and the ocular dominance distribution was similar to adults at all ages studied. These results indicate that many response properties of PMLS neurons are similar to those of adults as early as 2 weeks of age, soon after the time of eye opening. However, some properties show marked developmental changes. The mechanisms and sources of these changes are considered. In addition, the relevance of these results to mechanisms of compensation following early damage to visual cortical areas 17, 18 and 19 is discussed.

Binocular interactions in the cat's dorsal lateral geniculate nucleus, II: Effects on dominant-eye spatial-frequency and contrast processing

The present study tested the hypothesis that nondominant-eye influences on lateral geniculate nucleus (LGN) neurons affect the processing of spatial and contrast information from the dominant eye. To do this, we determined the effects of stimulating the nondominant eye at its optimal spatial frequency on the responses of LGN cells to sine-wave gratings of different spatial frequency and contrast presented to the dominant eye. Detailed testing was carried out on 49 cells that had statistically significant responses to stimulation of the nondominant eye alone. Spatial-frequency response functions to nondominant-eye stimulation indicated that the responses were spatially tuned, as reported previously (Guido et al., 1989). Optimal spatial frequencies through the nondominant eye were significantly correlated with the optimal spatial frequencies through the dominant eye (r = 0.54; P less than 0.0001), and the optimal spatial frequencies were fairly similar for the two eyes. Nondominant-eye stimulation changed the maximal amplitude of the fundamental (F1) response to dominant-eye stimulation for only about 45% (22 of 49) of the cells that responded to nondominant-eye stimulation alone. The response vs. contrast function through the dominant eye was altered for 73% of the cells (51% independent of spatial frequency). Three types of effects were observed: a change in the initial slope of the response vs. contrast function (contrast gain), a change in the response amplitude at which saturation occurred, or an overall change in response at all contrasts. The incidence of these changes was similar for X and Y cells in LGN layers A, A1, and C (only four W cells were tested). Nondominant-eye stimulation had little or no effect on the sizes or sensitivities of the receptive-field centers or surrounds for the dominant eye. In addition, nondominant-eye stimulation had little or no effect on optimal spatial frequency, spatial resolution, or the bandwidth of spatial-frequency contrast sensitivity curves for the dominant eye. Possible functions of binocular interactions in the LGN are considered. The present results suggest a role in interocular contrast-gain control. Interocular contrast differences can occur before the acquisition of binocular fusion, when the two eyes are viewing different aspects of a visual stimulus. Psychophysical and physiological studies suggest that an interocular mechanism exists to maintain relatively constant binocular interactions despite differences in interocular contrast. The present results suggest that at least part of this mechanism occurs in the LGN.