Perturbation-driven paradoxical facilitation of visuo-spatial function: Revisiting the 'Sprague effect'

Abstract

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.

Keywords: Cat; Conscious visual perception; Focal brain damage; Human; Intercollicular commissural interactions; Interhemispheric rivalry; Lesion inference; Mutual inhibitory projections; Non-invasive brain stimulation (NIBS); Paradoxical functional restoration; Paradoxical lesion effects; Posterior parietal cortex; Reversible cortical deactivations; Right hemisphere stroke; Spatial attention; Sprague effect; Thermal deactivations; Transcallosal interactions; Transcranial direct current stimulation (tDCS); Transcranial magnetic stimulation (TMS); Unilateral neglect; Visuo-spatial attention rehabilitation.