Paul Cornwell

Role of the superior colliculus in analyses of space: Superficial and intermediate layer contributions to visual orienting, auditory orienting, and visuospatial discriminations during unilateral and bilateral deactivations

The superior colliculus (SC) has been implicated in spatial analyses of the environment, although few behavioral studies have explicitly tested this role. To test its imputed role in spatial analyses, we used a battery of four spatial tasks combined with unilateral and bilateral cooling deactivation of the upper and intermediate layers of the superior colliculus. We tested the abilities of cats to orient to three different stimuli: (1) moving visual, (2) stationary visual, (3) stationary white‐noise aural. Furthermore, we tested the ability of the cats to discriminate the relative spatial position of a landmark. Unilateral cooling deactivation of the superficial layers of the SC induced a profound neglect of both moving and stationary visual stimuli presented in, and landmark objects located within, the contralateral hemifield. However, responses to auditory stimuli were unimpaired. Unilateral cooling deactivation of both the superficial and intermediate layers induced a profound contralateral neglect of the auditory stimulus. Additional and equivalent deactivation of the opposite SC largely restored orienting to either moving visual or auditory stimuli, and restored landmark position reporting to normal levels. However, during bilateral SC deactivation, orienting to the static visual stimulus was abolished throughout the entire visual field. Overall, unilateral SC deactivation results show that the upper and intermediate layers of the SC contribute in different ways to guiding behavioral responses to visual and auditory stimuli cues. Finally, bilateral superior colliculus deactivations reveal that other structures are sufficient to support spatial analyses and guide visual behaviors in the absence of neural operations in the superior colliculus, but only under certain circumstances. J. Comp. Neurol. 441:44–57, 2001.

Evidence for greater sight in blindsight following damage of primary visual cortex early in life

This review compares the behavioral, physiological and anatomical repercussions of lesions of primary visual cortex incurred by developing and mature humans, monkey and cats. Comparison of the data on the repercussions following lesions incurred earlier or later in life suggests that earlier, but not later, damage unmasks a latent flexibility of the brain to compensate partially for functions normally attributed to the damaged cortex. The compensations are best documented in the cat and they can be linked to system-wide repercussions that include selected pathway expansions and neuron degenerations, and functional adjustments in neuronal activity. Even though evidence from humans and monkeys is extremely limited, it is argued on the basis of known repercussions and similarity of visual system organization and developmental sequence, that broadly equivalent repercussions most likely occur in humans and monkeys following early lesions of primary visual cortex. The extant data suggest potentially useful directions for future investigations on functional anatomical aspects of visual capacities spared in human patients and monkeys following early damage of primary visual cortex. Such research is likely to have a substantial impact on increasing our understanding of the repercussions that result from damage elsewhere in the developing cerebral cortex and it is likely to contribute to our understanding of the remarkable ability of the human brain to adapt to insults.

Transneuronal degeneration of beta retinal ganglion cells in the cat.

Transneuronal retrograde degeneration of retinal ganglion cells was investigated following neonatal visual cortex ablation in the cat. After a survival time of at least 18 months, retinal ganglion cells projecting to the thalamus were labelled by retrograde transport of horseradish peroxidase. Filled ganglion cells were classified into α, β and γ types on the basis of dendritic morphology. In normal cats, α cells made up 8-10% of the total population in the sample area, β cells made up 64-67% and γ cells made up 23-27%. In retinae of visual cortex-ablated cats, normal numbers of α and γ cells were present, but the β cell population was depleted by 90% of normal. Thalamic projections of surviving retinal ganglion cells were investigated by anterograde transport of tritiated proline injected into the eye. In these animals, ablation of visual cortex resulted in almost complete degeneration of laminae A and A1 of the dorsal lateral geniculate nucleus. In the radioautographic material, projections from the retina to the degenerated parts of laminae A and A1 were barely detectable. Survival of some ganglion cell populations and death of others after neonatal visual cortex ablation may be explained in terms of the pattern of projections of the different cell types. We conclude that the majority of β cells degenerate following visual cortex ablation because of removal of cells in the dorsal lateral geniculate nucleus which form their sole or principal target. Alpha and γ cells and 10% of β-cells survive because of extensive collateral projections to targets other than cells of the laminae A and A1 of dorsal lateral geniculate nucleus.

System-wide repercussions of damage to the immature visual cortex

Damage of the primary visual cortex in mammals, including humans, severely disrupts vision by disconnecting much of the cognitive-processing machinery of extrastriate cortex from its source of visual signals in the retina. Studies of the anatomical consequences of damage to the immature primary visual cortex in cats reveal system-wide repercussions on neural circuitry that includes the retina, thalamus, midbrain and extrastriate cortex. The repercussions modify circuits that support relatively normal signal processing and the sparing of certain visually guided behaviors such as aspects of complex-pattern recognition and orienting to novel stimuli introduced into the visual field. These studies have implications for understanding the consequences of damage to the visual cortex in infant monkeys and humans, and for devising therapeutic strategies to attenuate defects in vision induced by cortical lesions.

Transneuronal retrograde degeneration in the cat retina following neonatal ablation of visual cortex

Bilateral removal of the cortical visual area in newborn cats produces degeneration of retinal ganglion cells. Measurements of over 4,000 cells and calculation of neuron densities from sample areas of retina in the adult show that the medium sized cell population in peripheral retina is reduced by 68%, whereas the populations of small and large cells are not affected. The degeneration is greater in peripheral retina than in area centralis.

Differential sparing of depth perception, orienting, and optokinetic nystagmus after neonatal versus adult lesions of cortical areas 17, 18, and 19 in the cat.

Performance by cats with lesions of the visual cortex made in infancy or adulthood was examined on tasks of visually guided behavior that do not require specific training. Cats with lesions confined to areas 17, 18, and 19 made during the 1st postnatal week showed more sparing of function on a visual cliff, at orienting to targets suddenly appearing in the visual field, and at optokinetic nystagmus than did cats with equivalent damage incurred as adults. Cats with lesions that included areas 17, 18, 19 and most of the contiguous visual areas were severely impaired at all tasks whether the lesions were incurred neonatally or in adulthood. These findings suggest that sparing of vision after neonatal lesions of cortical areas 17, 18, and 19 is not confined to pattern learning tasks and that remaining lateral cortical visual areas are importantly involved in such sparing.

Selective sparing after lesions of visual cortex in newborn kittens

Previous findings are discordant regarding the effects of perinatal lesions of Cortical Areas 17 and 18 on visual discrimination learning in cats. Three potential determinants of such sparing were investigated: age at lesion (4 or 181 days), age at testing (3 or 9 months), and stimulus complexity. Age at testing was not significant, but performance varied with stimulus complexity and cortical damage, and there was an interaction between stimulus complexity and age at lesion. Both operated groups were transiently impaired in discriminating objects and subsequently learned to discriminate simple 2-dimensional patterns as well as done by controls, but the lesion groups were permanently impaired in discriminating similar patterns circumscribed by irrelevant lines. The age-at-lesion groups differed, however, in discriminating patterns masked by superimposed lines. The group lesioned at 181 days was severely impaired at both acquisition and subsequent intercurrent performance; the group lesioned at 4 days was impaired only at intercurrent performance. This study suggests that sparing after early postnatal damage of Areas 17 and 18 occurs only under limited circumstances.

Neocortical connections in fetal cats

The major extrinsic projections to and from visual and auditory areas of cerebral cortex were examined in fetal cats between 46 and 60 days of gestation (E46-E60) using axonal transport of horseradish peroxidase either alone or in combination with tritiated proline. Projections to visual cortex from the dorsal lateral geniculate nucleus and lateral-posterior/pulvinar complex exist by E46, and those from the contralateral hemisphere, claustrum, putamen, and central lateral nucleus of the thalamus are present by E54-E56. In addition, cells in the medial geniculate nucleus project to auditory cortex by E55. At E54-E56 efferent cortical projections reach the contralateral hemisphere, claustrum, putamen, lateral-posterior/pulvinar complex and reticular nucleus of the thalamus. Cells in visual cortex also project to the dorsal and ventral lateral geniculate nuclei, pretectum, superior colliculus and pontine nuclei, and cells in auditory cortex project to the medial geniculate nucleus. Except for interhemispheric projections, all pathways demonstrated are ipsilateral, and projections linking cerebral cortex with claustrum, dorsal lateral geniculate nucleus and lateral-posterior/pulvinar complex are reciprocal. The reciprocal projections formed with the dorsal lateral geniculate nucleus, lateral-posterior/pulvinar complex and the claustrum show a greater degree of topological organization compared to the projections formed with the contralateral hemisphere and superior colliculus, which show little or no topological order. Therefore, the results of the present study show that the major extrinsic projections of the cats visual and auditory cortical areas with subcortical structures are present by the eighth week of gestation, and that the origins and terminations of many of these projections are arranged topologically.

Visual discrimination by cats given lesions of visual cortex in one or two stages in infancy or in one stage in adulthood

Sparing of visual function was studied in cats with bilateral cortical damage to Areas 17 and 18 and most of Area 19. Cats with lesions made in 2 stages, on Postnatal (P) Days 3 and 6, in 1 stage on P6, or in 1 stage in adulthood were compared with sham-operated controls on 10 visual discrimination tasks. On some tasks, both groups of cats that underwent surgery as infants showed considerable sparing of function compared with cats that had surgery as adults; the latter group showed a marked impairment. However, on several of the discriminations, 2-stage lesions permitted almost total sparing of pattern vision, whereas 1-stage lesions made neonatally were almost as debilitating as those incurred in adulthood. The findings suggest that differential behavioral consequences can follow physiological or anatomical changes, or both, that occur within a 4-day neonatal interoperative period.

Cortical lesions and response inhibition in cats

Abstract Groups of five cats each, with lesions in gyrus proreus, in the pericruciate area, and in both areas, were tested on 6 tasks yielding measures of perseveration and of deficiencies in response suppression. The animals with pericruciate lesions were inferior to normal controls only in the rate with which they extinguished responding in a runway. No evidence that pericruciate lesions exacerbate the effects of proreal lesions was obtained. Cats with proreus or combined lesions and severe retrograde degeneration in the mediodorsal nucleus showed marked impairments on all tasks studied. Subjects with proreal or combined lesions and less severe degeneration in MD showed similar but midler and more transient impairments on extinction and reversal tasks. Intercorrelations between seven measures of learning performance did not suggest that the behavioral impairments in the brain-injured cats could be explained in terms of the disruption of one or two pervasive forms of inhibition. An impairment in reversal learning in cats with of one or two pervasive forms of onhibition. An impairment in reversal learning in cats with lesions in the posterior association cortex involving Ep was also described.