Eye dominance modulates visuospatial attention

Highlights

• Eye dominance interacts with the right hemisphere dominance in attention.

• Eye dominance accounts for pseudoneglect phenomenon.

• Eye dominance influences spatial attention performance.

• Activation of primary visual areas influences spatial attention.

Abstract

Visuospatial attention has an inherent asymmetry: the leftward bias called pseudoneglect. In typical line bisection tasks, healthy individuals tend to judge the center of a line leftward of the true center, an effect attributed to the right hemisphere dominance in visuospatial attention. Since it has been shown that information perceived by the dominant eye strongly activates the ipsilateral visual cortex, we hypothesized that eye dominance may modulate visuospatial attention bias. Because activation of the left hemisphere induced by left eye dominance should mitigate the right hemisphere dominance in attention, we predicted that right-handed individuals with left dominant eye would show smaller amount of pseudoneglect than right-handed individuals with right dominant eye. We compared the performance at both the perceptual (Landmark) and manual line bisection task of forty right-handed healthy individuals, half of whom had a right dominant eye and the other half a left dominant eye. As predicted, the left eyed dominant group showed smaller, actually not significant pseudoneglect, which was thus greater in the right eye dominant group. The influence of eye dominance on visuospatial attention was present in the Landmark but not the manual line bisection task, in which the amount of visuospatial bias correlated with participants’ degree of (right) handedness. This is the first report of the effect of eye dominance on visuospatial attention within a right-handed population. This finding, by showing the influence of eye dominance on visuospatial cognition, not only helps in better defining intact visuospatial cognition mechanism but also encourages further research to pinpoint the neural basis of such interaction.

Introduction

Young individuals free of neurological disorders usually judge the center of a line leftward of the true center as measured by line bisection tasks (Milner et al., 1992; Schenkenberg et al., 1980). This leftward bias in intact visuospatial attention is called pseudoneglect (Bowers and Heilman, 1980; for a review see Jewell and McCourt, 2000). Pseudoneglect is hypothesized to be the product of the uneven distribution of attention due to the right hemispheric dominance in attention (Kinsbourne, 1970, Mesulam, 1999, Nicholls and Roberts, 2002). The right hemisphere is indeed the most activated one during attentional task and, as the activation-orientation theory posits, this increased attention to the contralateral (left) hemifield makes the left visual space (i.e., left side of the line) being perceived longer then the right one, and thus judging the center of line leftward of the true center (Bultitude and Aimola Davies, 2006).

Pseudoneglect is typically present at the population level, but much inter individual variability is observed (Manning et al., 1990; McCourt and Olafson, 1997; Jewell and McCourt, 2000; Toba et al., 2011; Szczepanski and Kastner, 2013). Among the several factors influencing spatial attention performance, such as handedness strength (Ochando and Zago, 2018), eye dominance is gaining increasing interest (e.g., Roth et al., 2002; Szczepanski and Kastner, 2013). Eye dominance and handedness have been shown to have a very weak relationship, with 66% of right-handers having a right DE and 60% of left-handers having a left DE (Bourassa et al., 1996). Numerous studies failed to show a clear link between the two, which is not surprising given the fact the afference/efference of one hand is associate to one hemisphere whereas the efference of one eye is associated to both hemispheres (Mapp et al., 2003). The dominant eye is defined as the eye manifesting physiological superiority and it is the one chosen to align a target in peripersonal space with a more distant point, or when performing a monocular task such as looking through a small hole (it is referred to as sighting dominant eye; Porac and Coren, 1976). There are interocular differences in activation of visual areas in response to stimuli presented to the contralateral visual field, with the dominant eye generating a stronger activation in response to sensory information as compared to the one generated by the non-dominant one (Mendola and Conner, 2007; Rombouts et al., 1996). Since the dominant eye, as compared to the non-dominant one, activates larger portions of the ipsilateral primary visual cortex (Erdogan et al., 2002), it has been concluded that ocular dominance is mainly depending on the ipsilateral occipital lobe (Shima et al., 2010) possibly as a result of more numerous, or stronger inputs gathered by the temporal hemiretina and projecting to the ipsilateral visual cortex. Consistent with this last proposition, simple reaction times in response to a lateralized visual target are shorter for the contralateral visual hemifield with respect to the DE (Chaumillon et al., 2014). Globally, there is an advantage for stimuli processed by the dominant eye: perceived image size is increased (Coren and Porac, 1976) and percept is more salient, suggesting that information from the dominant eye has priority in visual processing (Shneor and Hochstein, 2008, 2006).

Grounding on the activation-orientation theory (Reuter-Lorenz et al., 1990) we hypothesized that eye dominance may impact physiologically visuospatial attention bias, and namely that individuals with right dominant eye should show a greater amount of pseudoneglect as compared to individuals with a left dominant eye. The activation-orientation theory, by postulating that the distribution of attention is biased toward the direction opposite to the most activated hemisphere, accounts for the pseudoneglect phenomenon as due to a biased perception of the half of the line in the left hemifield because of the right hemisphere dominance for visuospatial attention. We predicted that right-handed individuals with right dominant eye, as compared to right-handed individuals with left dominant eye, should show a greater amount of pseudoneglect. This would depend on of the fact that information from the left side of the line is perceived elongated because it is processed by the right hemisphere, which not only is the most activated by the attentional task, but also by the inputs of their right dominant eye to the right visual cortex (i.e., right hemisphere dominance plus dominant eye). By contrast, in individuals with left dominant eye, the leftward bias would be mitigated by the activation of the left hemisphere due to stronger inputs from the left dominant eye to the left visual cortex. We thus put forward here a simple model to predict the manifestation of pseudoneglect as a function of eye dominance: left eye dominance, by increasing the activity in the left visual cortex, would dampen the typical bias depending upon right hemisphere dominance. We tested this prediction by comparing the performance at both the perceptual (Landmark) and manual line bisection tasks, between one group of healthy right-handed participants with right dominant eye and one group of healthy right-handed participants with left dominant eye. These tasks, despite being both used to quantify visuospatial asymmetry (Zago et al., 2017), bear substantial differences (Milner et al., 1992). The Landmark task can be summarized as a pure test of perceptual/attentional bias, as it requires to judge a series of pre-bisected lines and, in our study, avoids any hand movement, whereas the motor line bisection task involves motor bias by requiring to actively bisect a line with the dominant hand. We therefore expect eye dominance and strength of handedness to have a different weight in the quantification of the visuospatial bias according to the task used to measure it. We predict eye dominance to manifest its influence on visuospatial bias when assessed in the more perceptual manner, i.e., the Landmark task, and handedness to show its influence on visuospatial bias when assessed by manual line bisection because of the motor bias intrinsic to the task.

Our model and predictions were supported by the results, showing that eye dominance contributes in determining the presence and amount of pseudoneglect in the precited direction solely when assessed by the Landmark task. This finding may help account for the inter-individual variability observed in the pseudoneglect phenomenon.