Visual function within the hemianopic field following early cerebral hemidecortication in man—I. Spatial localization

doi:10.1016/0028-3932(78)90037-4

Neuropsychologia

Volume 16, Issue 1, 1978, Pages 1-13

https://doi.org/10.1016/0028-3932(78)90037-4 Get rights and content

Abstract

Localization abilities within the hemianopic field have been tested in 6 subjects hemidecorticated in early life for infantile hemiplegia-epilepsia. Two other Ss suffering from a pregeniculate (chiasmatic) lesion of visual pathways served as controls. In hemidecorticated Ss, a significant correlation was found between the position of bright targets within the hemianopic field, and the position of corresponding hand pointings. This was not the case in control Ss. In addition, the ocular responses to brief target exposures in the hemianopic field tested in two hemidecorticated Ss, were also significantly related to target position. These results suggest that location of visual stimuli can still be estimated in parts of the visual field which are no longer controlled by cortical areas and that, according to experimental data, the superior colliculus should be responsible for this residual spatial ability.

Résumé

Les capacités de localisation spatiale à l'intérieur du champ hémianopsique ont été testées chez 6 sujets ayant subi une hémidécortication précoce pour hémiplégie cérébrale infantile-épilepsie. Deux autres sujets porteurs d'une lésion prégéniculée (chiasmatique) des voies visuelles ont été testés en outre comme controle. Chez les sujets hémidécortiqués a été constatée une relation significative entre la position de cibles lumineuses à l'intérieur du champ hémianopsique et la position des pointers de la main en réponse à ces cibles. Cette relation n'a pas été retrouvée par contre chez les sujets de controle. Cette relation n'a pas été retrouvée par contre chez les sujets de controle. En outre, les réponses oculomotrices à l'apparition brève des cibles dans le champ hémianopsique, testées chez deux sujets hémidécortiqués, étaient aussi reliées de facon significative à la position de la cible. Ces résultats indiquent donc la persistance de capacités de localisation spatiale dans des zones du champ visuel n'étant plus controlées par le cortex et suggèrent, en accord avec des données expérimentales, que le colliculus supérieur pourrait en etre responsable.

Zusammenfassung

Bei 6 Patienten, die in der Kindheit wegen früh erworbener Hemiplegie und Epilepsie decorticalisiert worden waren, wurde die Fähigkeit, im hemianopischen Gesichtsfeld zu lokalisieren, untersucht. Zwei weitere Patienten, deren optische Bahnen vor dem Geniculatum laediert waren, dienten als Kontrollen. Bei den hemidocorticalisierten Patienten fand sich eine signifikante Korrelation zwischen den Orten der im hemianopischen Gesichtsfeld gebotenen hellen Punkte und den Orten, auf die die Patienten bei ihrer Antwort zeigten. Das war nicht der Fall bei den Kontrollpersonen.

Auβerdem standen bei zwei entsprechend untersuchten hemidecorticlaisierten Patienten die oculären Reaktionen auf im hemianopischen Feld kurz dargebotene Punkte in signifikanter Weise in Beziechung zum Ort des Zielpunktes.

Diese Ergebnisse sprechen dafür, daβ die Orte von visuellen Stimuli in Gesichtsfeldabschnitten, die nicht mehr von corticalen Bezirken kontrolliert werden in etwa noch angegeben werden können, und daβ nach den experimentellen Daten der obere Colliculus für die Restfähigkeit zu lokalisieren verantwortlich sein dürfte.

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Citation Excerpt :
Patients vary widely in the range of residual blindsight abilities they have, which may reflect the fact that different forms of blindsight are supported by different neural pathways, which will be affected variably by different lesions in different patients. In the early work of Marie-Thérèse Pérenin and Marc Jeannerod (Perenin and Jeannerod, 1975, 1978; Perenin, 1978), patients could reach accurately to targets without being able to identify their shape, and similar dissociations were found in some of their hemidecorticated patients (Perenin, 1978; Perenin and Jeannerod, 1978). A related dissociation was also reported between prehension parameters (size and orientation) and corresponding perceptual characteristics (Perenin and Rossetti, 1996).
For over a century, research has demonstrated that damage to primary visual cortex does not eliminate all capacity for visual processing in the brain. From Riddoch's (1917) early demonstration of intact motion processing for blind field stimuli, to the iconic work of Weiskrantz et al. (1974) showing reliable spatial localization, it is clear that secondary visual pathways that bypass V1 carry information to the visual brain that in turn influences behavior. In this chapter, we briefly outline the history and phenomena associated with blindsight, before discussing the nature of the secondary visual pathways that support residual visual processing in the absence of V1. We finish with some speculation as to the functional characteristics of these secondary pathways.
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Accuracy of saccades and hand reaches is poorer than in their healthy visual field and in healthy subjects, but it is significantly better than chance, i.e. the saccade or reach endpoints are correlated with target positions. It has been proposed that subcortical substrates such as the superior colliculus may be responsible for this residual visuo-motor ability (Weiskrantz et al., 1974; Zihl and Werth, 1984a, 1984b), which is directly supported by the observation of blindsight in patients with hemispherectomy (Perenin and Jeannerod, 1978), by functional brain imaging (Leh et al., 2010) and correlation between blindsight occurrence and pupillary reactions (Sahraie et al., 2013). However the accuracy of pointing movements appears to be better than that of saccades performed by some blindsight patients (Danckert and Rossetti, 2005).
Blindsight has been primarily and extensively studied by Lawrence Weiskrantz. Residual visual abilities following a hemispheric lesion leading to homonymous hemianopia encompass a variety of visual-perceptual and visuo-motor functions. Attention blindsight produces the more salient subjective experiences, especially for motion (Riddoch phenomenon). Action blindsight illustrates visuo-motor abilities despite the patients’ feeling that they produce random movements. Perception blindsight seems to be the weakest residual function observed in blindsight, e.g. for wavelength sensitivity. Discriminating motion produced by isoluminant colours does not give rise to blindsight for motion but the outcome of the reciprocal test is not known. Here we tested whether moving stimuli could give rise to colour discrimination in a patient with homonymous hemianopia. It was found that even though the patient exhibited nearly perfect performances for motion direction discrimination his colour discrimination for the same moving stimulus remained at chance level. It is concluded that easily discriminated moving stimuli do not give rise to colour discrimination and implications for the 3 levels of blindsight taxonomy are discussed.
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Blindsight, the residual abilities of patients with cortical blindness to respond proficiently to stimuli they do not consciously acknowledge, offers a unique opportunity to study the functional and anatomical mechanisms sustaining visual awareness. Over decades, the phenomenon has been documented in a wide number of different patients, across independent laboratories, and for a variety of tasks and stimulus properties. Nevertheless, the functional neuroanatomy of blindsight remains elusive and alternative proposals have been put forth. To tackle this issue from a novel perspective, we performed a quantitative Activation Likelihood Estimation (ALE) meta-analysis on the neuroimaging literature available on blindsight. Significant activity was reported in subcortical structures, such as the superior colliculus, pulvinar and amygdala, as well as in cortical extrastriate areas along the dorsal and ventral visual stream. This data-driven functional network collectively defines the extant neural fingerprint of blindsight. To further characterize the unique combination of segregation and integration in brain networks engaged in blindsight, we measured the relationship between active areas and experimental features in the original studies, their clustering and hierarchical organization. Results support a network-based organization in the functional neuroanatomy of blindsight, which likely reflects the intersection of different stimulus properties and behavioural tasks examined. We suggest that the conceptualization of blindsight as a constellation of multiple nonconscious visual abilities is better apt as a summary of present-day wisdom, thereby mirroring the variety of existing V1-independent pathway and their different functional roles.

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Visual function within the hemianopic field following early cerebral hemidecortication in man—I. Spatial localization

Abstract

Résumé

Zusammenfassung

Prog. Brain Res.

Neuropsychologia

Neuropsychologia

Expl. Neurol.

Brain Res.

Infantile hemiplegia treated by removal of one cerebral hemisphere

J. Neurol. Neurosurg. Psychiat.

Cerebral hemispherectomy: present status and clinical indications

Neurology

L'hémisphérectomie

Nervous integration after hemispherectomy in man

Cerebral hemispherectomy for infantile hemiplegia

Brain

Nervous function after right hemispherectomy

Neurology

Visual function in patients with homonymous hemianopia—I. The visual fields

Brain

Residual visual function after brain wounds involving the central visual pathways in man

Nature, Lond.

Visual capacity in the hemianopic field following a restricted occipital ablation

Brain

Visuo-motor function in the cerebral cortex

J. nerv. ment. Dis.