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The Nature of Foveal Representation Projections from the Nasal Part of the Retinae to Reach the Ipsilateral Hemispheres

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The Nature of Foveal Representation Projections from the Nasal Part of the Retinae to Reach the Ipsilateral Hemispheres PERSPECTIVES OPINION hemiretina, project to the ‘wrong’ laminae of the LGN. These results were taken to show that the crossing of the nasal retinal fibres in the optic chiasm is incomplete, allowing some The nature of foveal representation projections from the nasal part of the retinae to reach the ipsilateral hemispheres. Normally, Michal Lavidor and Vincent Walsh however, foveal stimuli received by the nasal retinae are projected to the contralateral visual Abstract | A fundamental question in visual the visual midline. This is what Descartes1 cortex. A later study10 indicated that the perception is whether the representation of suggested in his description of the visual dendritic coverage of the centre of the fovea the fovea is split at the midline between the system — he identified the pineal gland as the by RGCs provides a possible neural basis for two hemispheres, or bilaterally represented organ of integration (FIG. 1).Unfortunately, 2–3° of bilateral representation of the fovea by overlapping projections of the fovea in this intuitive, appealing explanation is in the central visual pathways. There is also each hemisphere. Here we examine not true, and we therefore have to assume evidence that the nasotemporal overlap psychophysical, anatomical, that the two cerebral hemispheres cooperate increases towards the upper and lower regions neuropsychological and brain stimulation or compete over the representation of the of the retina11. experiments that have addressed this human foveal area. Most studies that have labelled RGCs with question, and argue for a shift from the When a person is fixating centrally (looking HRP after unilateral injections into the mon- current default view of bilateral straight ahead), information that is to key optic tract have found a nasotemporal representation to that of a split the right of fixation (in the right visual field) is overlap zone along the vertical meridian12. representation, to provide a greater projected to the visual cortex of the left However, Tootell et al.13 injected the optic 14 understanding of higher visual processes. cerebral hemisphere, and information that is to tract of monkeys with [ C]2-deoxy-D-glucose the left of fixation (in the left visual field) (2DG) and presented stimuli at various loca- Basic anatomical facts dictate that what is projected to the visual cortex of the right tions in their visual fields, including some appears as a whole percept (a foveally fixated cerebral hemisphere. However, it is not entirely stimuli presented only 0.15° from the vertical target) is in fact represented by separate entities clear how the visual half-fields flank one meridian. If the close-to-fixation targets are — the two cerebral hemispheres — at the early another along the vertical meridian2 to bilaterally projected, then they should activate stages of cortical processing. The often-ignored represent the foveal area — the central 2° of neurons in the primary visual cortex on both question of how the two hemispheres repre- the retina3.The bilateral projection theory sug- sides of the brain, and both sides should sent foveal stimuli in the human brain is the gests that the representation of foveal stimuli is become labelled with 2DG. However, only the focus of this article. We also look at the poten- projected to both hemispheres (with various hemisphere opposite to the stimulated visual tial implications of foveal representation for degrees of overlap). Alternatively, the foveal field was labelled, even for targets close to models of visual cognition. representation could be entirely split between fixation. The authors concluded that this Models that use word or object recognition the two hemispheres, as proposed by the split evidence was inconsistent with a bilateral usually begin by assuming that the ‘simple’ fovea theory. It is a textbook assumption representation of the foveal area13. task of bringing together the two retinal that the visual fields overlap according to the Functional anatomical studies of humans outputs has been achieved by the occipital bilateral projection theory 4,and therefore little also support the split foveal theory. Given the cortex before the more interesting psycho- attention is paid to evidence that supports cortical magnification of the fovea14 and the logical processes begin. However, it is becom- a split. It is this assumption that we wish to limited ability of humans to fixate stably15, it is ing increasingly clear that the assumptions challenge. difficult to investigate foveal representation made about retinal representation of the fovea using brain imaging (such as functional MRI severely constrain the degrees of freedom Anatomical studies (fMRI)), as the fMRI signal becomes increas- available in such models. The important theo- The first direct anatomical evidence for hemi- ingly sensitive to inaccurate fixation the closer retical question is whether visual processing spheric overlap of the visual representation one gets to the fovea16.For this reason, stimuli at higher levels might be influenced or con- along the vertical meridian came from studies are often presented at least 0.5° away from the strained by theoretical concerns that are based in which horseradish peroxidase (HRP) was vertical meridian17,18. on either a split foveal representation or a injected unilaterally into the dorsal lateral However, some recent brain imaging studies bilateral projection of the retinal images onto geniculate nucleus (dLGN) of cats or mon- might be interpreted as supporting the split the visual cortex. Recent advances in this field keys to trace the projections from the retinal foveal theory. In a magnetoencephalographic allow us to reassess this issue and to present ganglion cells (RGCs)5–8.Ifthe optic fibres (MEG) study15,18,Portin and colleagues pre- the implications of this relatively low-level split precisely, the prediction would be that sented visual stimuli at different eccentricities question for theories of higher-level visual only cells in one half of each retina would (0.5–6.0°), which evoked strong responses in representation. be stained: for example, injections into the contralateral occipital cortex. Stimuli at all the right LGN should stain cells in the tempo- of these eccentricities evoked activity only Views of foveal representation ral hemiretina of the right eye and the nasal in the contralateral primary visual cortex, as It has long been known that visual acuity is hemiretina of the left eye2.Contrary to this predicted by the split fovea theory. If there best when the target is presented at the point prediction, these studies have found that were a bilateral foveal representation, targets in of fixation. Given the organization of the ipsilaterally and contralaterally projecting the foveal area should have activated both optic nerves, an intuitive explanation for this ganglion cells generally blend together along hemispheres. Similarly, in an fMRI study, increased acuity would be that there must be the vertical midline. Leventhal et al.9 reported Sereno et al.17 mapped the representation of a central brain structure that corresponds to that some RGCs, particularly those in the nasal different eccentricities in the visual cortex, and NATURE REVIEWS | NEUROSCIENCE VOLUME 5 | SEPTEMBER 2004 | 729 PERSPECTIVES Hemispheric differences Despite the anatomical and neurological evidence for the split fovea theory, the concept failed to take hold in experimental psychol- ogy, and many studies still implicitly assume that there is a bilateral representation. This is partly because more lateral presentations of stimuli make eye movement artefacts easier to avoid. However, the split fovea theory has inspired recent studies of human cognition. The starting point was to look at established hemispheric differences in cognition and to test whether they could be applied to the left and right halves of centrally presented words. Figure 1 | The projection of visual foveal stimuli to the pineal gland (Descartes, 1644). In The The hypothesis was that, according to the split 1 Philosophical Writings of Descartes , Descartes wrote (105–106), ‘The rays which come from point B fovea theory, aspects of word recognition that [arrow centre] enlarge the openings of the tiny tube 4…suppose next that the spirits [from the pineal gland] tend to enter each of the tiny tubes…those spirits coming from point b [pineal gland centre] tend to enter are more characteristic of the right hemi- tubes 4…Thus, just as a figure corresponding to point B is traced on the internal surface of the brain sphere would be found for the processing of according to the different ways in which tubes 4 are opened, likewise that figure is traced on the surface of the left halves of centrally presented words. the pineal gland according to the ways which the spirits leave from point b.’ Correspondingly, patterns that are typical of the left hemisphere should be found for the processing of the right halves of words. also found that positions to the left of fixation of a split fovea has simply not stuck. Perhaps One variable that demonstrates the value are represented only in the right primary visual the body of evidence that has contributed most of this approach is word length (number of cortex and vice versa (FIG. 2). to the persistence of the bilateral projection letters), which has been reported to have theory is that of patients with visual cortex different effects in the two hemispheres, such Human behavioural studies damage, which is discussed next. that performance measured by response Studies of human behaviour conducted in the times deteriorated with increasing word 1970s and 1980s showed that there is no func- Foveal sparing and foveal splitting length in the left, but not the right, visual tional overlap between the two hemispheres in Unilateral lesions in the central visual pathways field38–40.The split fovea theory predicts length relation to the representation of foveal stimuli. can result in two qualitatively different central effects for the letters to the left of fixation, but For example, Harvey19 presented visual targets visual field defects — foveal (or macular) not for the letters to the right of fixation.
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