Oculomotor Functions of the Parietal Lobe: Effects of Chronic Lesions in Humans

doi:10.1016/S0010-9452(08)70411-8

Cortex

Volume 42, Issue 5, 2006, Pages 730-739

https://doi.org/10.1016/S0010-9452(08)70411-8 Get rights and content

Abstract

This review summarises research in patients with chronic lesions of parietal oculomotor cortex and compares their oculomotor performance to patients with lesions of the frontal eye field (FEF). The observations identify the oculomotor functions for which these regions are indispensable, and explore dynamic interactions within cortical and subcortical networks for oculomotor control. The experiments examined endogenously generated saccades, saccades to visual targets, antisaccades, saccade choice and saccade remapping for inhibitory spatial tagging. The findings suggest that the key function of parietal oculomotor cortex is the computation of sensorimotor transformations, rather than the initiation of either voluntary or reflexive saccades. They also reveal the re-organisation of cortico-subcortical networks after brain injury, and provide insight into their dynamic interactions: FEF lesions result in disinhibition of reflexive saccades toward the contralesional field and an impairment of reflexive saccades toward the ipsilesional field; whereas parietal lesion result in the opposite pattern.

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Scene construction is a key component of memory recall, navigation, and future imagining, and relies on the medial temporal lobes (MTL). A parallel body of work suggests that eye movements may enable the imagination and construction of scenes, even in the absence of external visual input. There are vast structural and functional connections between regions of the MTL and those of the oculomotor system. However, the directionality of connections between the MTL and oculomotor control regions, and how it relates to scene construction, has not been studied directly in human neuroimaging. In the current study, we used dynamic causal modeling (DCM) to interrogate effective connectivity between the MTL and oculomotor regions using a scene construction task in which participants’ eye movements were either restricted (fixed-viewing) or unrestricted (free-viewing). By omitting external visual input, and by contrasting free- versus fixed- viewing, the directionality of neural connectivity during scene construction could be determined. As opposed to when eye movements were restricted, allowing free-viewing during construction of scenes strengthened top-down connections from the MTL to the frontal eye fields, and to lower-level cortical visual processing regions, suppressed bottom-up connections along the visual stream, and enhanced vividness of the constructed scenes. Taken together, these findings provide novel, non-invasive evidence for the underlying, directional, connectivity between the MTL memory system and oculomotor system associated with constructing vivid mental representations of scenes.
Rightward exogenous attentional shifts impair perceptual memory of spatial locations in patients with left unilateral spatial neglect
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Spatial remapping implies the updating and maintaining of the spatial position of objects in successive visual images across time, despite their displacement on the retina due to eye movements. In the parietal cortex, the representation of spatial locations appears to be partly centered on gaze direction, and thus modulated by current eye-gaze position. It has been suggested that short-term memory for spatial locations across delays might be impaired in right brain-injured patients with left spatial neglect, but more so after rightward than leftward gaze shifts – an asymmetry attributed to a loss of spatial representations normally transferred from left to right hemisphere during remapping. Because several studies point to a strong link between attentional and oculomotor circuits in the brain, we hypothesized that similar remapping effects might result from attentional displacements without overt eye movements. We tested this hypothesis in right-brain damaged patients with and without left neglect in a visuo-spatial memory task. As predicted, neglect patients showed a selective deficit in location memory following an exogenous attentional shift caused by a brief flash in the periphery of their right (but not left) visual field. We conclude that an attentional displacement without eye movements is sufficient to remap spatial representations across hemifields, and that this process is impaired in neglect patients when a location has to be transferred to the neglected/left side relative to current gaze or attention focus. More generally, these results support the notion of neural overlap between oculomotor and attentional mechanisms, and confirm a role for impaired remapping in the neglect syndrome, wherein spatial representations of contralesional locations may fail to be maintained during active attentional behavior.
Perturbation-driven paradoxical facilitation of visuo-spatial function: Revisiting the ‘Sprague effect’
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The ‘Sprague Effect’ described in the seminal paper of James Sprague (Science 153:1544–1547, 1966a) is an unexpected paradoxical effect in which a second brain lesion reversed functional deficits induced by an earlier lesion. It was observed initially in the cat where severe and permanent contralateral visually guided attentional deficits generated by the ablation of large areas of the visual cortex were reversed by the subsequent removal of the superior colliculus (SC) opposite to the cortical lesion or by the splitting of the collicular commissure. Physiologically, this effect has been explained in several ways-most notably by the reduction of the functional inhibition of the ipsilateral SC by the contralateral SC, and the restoration of normal interactions between cortical and midbrain structures after ablation. In the present review, we aim at reappraising the ‘Sprague Effect’ by critically analyzing studies that have been conducted in the feline and human brain. Moreover, we assess applications of the ‘Sprague Effect’ in the rehabilitation of visually guided attentional impairments by using non-invasive therapeutic approaches such as transcranial magnetic stimulation (TMS) and transcranial direct-current stimulation (tDCS). We also review theoretical models of the effect that emphasize the inhibition and balancing between the two hemispheres and show implications for lesion inference approaches. Last, we critically review whether the resulting inter-hemispheric rivalry theories lead toward an efficient rehabilitation of stroke in humans. We conclude by emphasizing key challenges in the field of ‘Sprague Effect’ applications in order to design better therapies for brain-damaged patients.
Oculomotor control after hemidecortication: One hemisphere encodes normal ipsilateral oblique anti-saccades
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A critical question in neurology is how the brain reorganizes its structure and function following injury. Here, we consider oculomotor control following a massive brain lesion, a hemispherectomy. We used the oblique anti-saccade task which requires the suppression of a saccade towards a visual cue, flashed anywhere in a patient's seeing hemifield, and the generation, in the dark, of an anti-saccade to a task-dependent location in the opposite blind hemifield; inverting either the horizontal or both horizontal and vertical components. Anti-saccades require a visuo-motor vector inversion that normally involves bilateral interactions between frontal, parietal and subcortical structures across both hemispheres. Here, oblique anti-saccades presented a major challenge to the patient's single hemisphere, requiring one site in visual cortex to communicate with an instruction-dependent site in oculomotor cortex. Patients with discrete frontal lobe damage can be strongly impaired in anti-saccades. By contrast, hemispherectomy patients performed oblique anti-saccades normally, contrasting with their permanent contralesional hemianopia and severe hemiparesis.
The Dorsal Frontoparietal Network: A Core System for Emulated Action
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Citation Excerpt :
Unilateral damage to the intraparietal cortex [98] or FEF [99] leads to delayed and hypometric contralesional saccades, but the reasons for these modifications appear to be different. While patients with parietal damage fail to compute target position in retinocentric coordinates, PMd damage affects the maintenance [100,101] and voluntary triggering [98,102] of motor plans necessary to initiate saccades. A more severe oculomotor impairment is observed following bilateral PPC damage.
The dorsal frontoparietal network (dFPN) of the human brain assumes a puzzling variety of functions, including motor planning and imagery, mental rotation, spatial attention, and working memory. How can a single network engage in such a diversity of roles? We propose that cognitive computations relying on the dFPN can be pinned down to a core function underlying offline motor planning: action emulation. Emulation creates a dynamic representation of abstract movement kinematics, sustains the internal manipulation of this representation, and ensures its maintenance over short time periods. Based on these fundamental characteristics, the dFPN has evolved from a pure motor control network into a domain-general system supporting various cognitive and motor functions.
Saccade abnormalities associated with focal cerebral lesions – How cortical and basal ganglia commands shape saccades in humans
2016, Clinical Neurophysiology
To study saccade abnormalities associated with focal cerebral lesions, including the cerebral cortex and basal ganglia (BG).
We studied the latency and amplitude of reflexive and voluntary saccades in 37 patients with focal lesions of the frontal and parietal cortices and BG (caudate and putamen), and 51 age-matched controls, along with the ability to inhibit unwanted reflexive saccades.
Latencies of reflexive saccades were prolonged in patients with parietal lesions involving the parietal eye field (PEF), whereas their amplitude was decreased with parietal or putaminal lesions. In contrast, latency of voluntary saccades was prolonged and their success rate reduced with frontal lesions including the frontal eye field (FEF) or its outflow tract as well as the dorsolateral/medial prefrontal cortex, and caudate lesions, whereas their amplitude was decreased with parietal lesions. Inhibitory control of reflexive saccades was impaired with frontal, caudate and, less prominently, parietal lesions.
PEF is important in triggering reflexive saccades, also determining their amplitude. Whereas FEF and the caudate emit commands for initiating voluntary saccades, their amplitude is mainly determined by PEF. Commands not only from FEF and dorsolateral/medial prefrontal cortex but also from the caudate and PEF serve to inhibit unnecessary reflexive saccades.
The findings suggested how cortical and BG commands shape reflexive and voluntary saccades in humans.

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Special SectionOculomotor Functions of the Parietal Lobe: Effects of Chronic Lesions in Humans

Abstract

Cognition

Behavioral Brain Research

Brain Research

Neuropsychologia

Neuropsychologia

Neuropsychologia

Extinction and stimulus repetition

Journal of Cognitive Neuroscience

Oculocentric spatial representation in parietal cortex

Cerebral Cortex

The functional anatomy of frontal lobe neglect in monkeys: Behavioral and 2-deoxyglucose studies

Annals of Neurology

Saccadic dysmetria in a patient with a right frontoparietal lesion

Brain

On the normal use of reflexes

American Scientist

Spatial attention deficits in humans: A comparison of superior parietal and temporal-parietal junction lesions

Neuropsychology

Effects of parietal lesions on visual matching: Implications for reading errors

Cognitive Neuropsychology

The parieto-collicular pathway: Anatomical location and contribution to saccade generation

European Journal of Neuroscience

Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task

Nature Neuroscience

Cortical control of double-step saccades: Implications for spatial orientation

Annals of Neurology

Endogenously generated and visually guided saccades after lesions of the human frontal eye fields

Journal of Cognitive Neuroscience

Impaired spatial working memory across saccades contributes to abnormal search in parietal neglect

Brain

Evolutionary perspectives on the function of the optic tectum

Brain Behavior and Evolution

Inhibition of return is a foraging facilitator in visual search

Psychological Science

Control of fixation and saccades during an anti-saccade task: An investigation in humans with chronic lesions of oculomotor cortex

Experimental Brain Research

Control of fixation and saccades in humans with chronic lesions of oculomotor cortex

Neuropsychology

Preattentive filling-in of visual surfaces in parietal extinction

Science

Special Section
Oculomotor Functions of the Parietal Lobe: Effects of Chronic Lesions in Humans