PLoS One. 2016 Dec 14;11(12):e0167646. doi: 10.1371/journal.pone.0167646.

Attentional Selection Accompanied by Eye Vergence as Revealed by Event-Related Brain Potentials.

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New role for eye vergence

Our eyes receive a slightly different projection of the image because of the different positions on the head. Therefore when looking at an object, the eyes must rotate around a vertical axis in order to have the projection of the image is in the center (fovea) of both retinas. Vergence refers to the simultaneous movement of both eyes in opposite directions to obtain single binocular vision (Fig. 1). Convergence is the simultaneous inward movement of both eyes toward each other, and divergence the simultaneous outward movement of both eyes. Due to the different viewpoints observed by the left and right eye, many other points in space do not fall on corresponding retinal locations. Visual binocular disparity defines this difference between the points of projection in the two eyes. The brain uses this binocular disparity to extract depth information from the two-dimensional retinal images. For this reason eye vergence is considered to be an important visual cue in depth perception.

 

We recently found an unpredicted but clear relation of eye vergence with attention and perception [Solé Puig et al., 2013]. We showed that during gaze fixation visual stimuli modulate the angle of eye vergence as a function of their ability to capture attention (Fig. 1). Vergence responses correlate with bottom-up and top-down attention. A role of eye vergence in attention is further supported by our studies showing that the EEG component that specifically signals visual attention correlates with eye vergence.

 

 

Figure 1. Schematic explanation of vergence and vergence responses during an attention task. The subject focusses on a single point in space where the angle of vergence is formed by the two gaze lines. When covertly paying attention to one of the vertical bars (target stimulus), vergence responses are observed.

 

Diagnostic support tool for ADHD

Attention deficit hyperactivity disorder (ADHD) is one of a common neurodevelopmental disorder affecting 3 to 7% of school-aged children worldwide. The diagnosis of ADHD is clinical based upon criteria established by classification systems such as the DSM-V. Even though the clinical diagnosis shows considerable levels of concurrent and predictive validity concerns persist, and additional tools are needed to support ADHD diagnosis. It is characterized by a low degree of attention, a high degree of hyperactivity and impulsivity, and the inability to inhibit inappropriate actions.

 

The altered behavior of ADHD patients is not limited to general conduct but it is also observed at the level of oculomotor behavior. ADHD patients have more difficulty suppressing saccadic eye movements when fixation is required (Karatekin and Asarnow, 1999) and the rate of micro-saccades is reported to be different in ADHD subjects compared to controls (Fried et al., 2014; Engbert and Kliegl, 2003). The poor eye control of ADHD patients is furthermore expressed as an increased variability in the latencies of saccadic responses to visual stimuli compared to healthy controls (Leth-Steensen et al., 2001). Besides the saccadic eye movements, dis-conjugate eye movements or vergence, i.e. where the eyes move in opposite direction (Fig. 1a) are affected in ADHD patients (Solé Puig et al., 2013; 2015).

 

 

Figure 2. ADHD study in children. Left upper panel show set-up and the right lower panel the child friendly ADHD task.  Average modulation of the angle of vergence. Phases in the task are demarcated by vertical lines. The lower dots indicate the time points when vergence responses significantly (p>0.05) differ between healthy and ADHD subjects and Clinical controls and ADHD subjects.

 

We tested whether vergence assessment can be used as a diagnostic tool for ADHD. We applied a child friendly attention task for ten minutes and recorded eye position data from which vergence was calculated. The principal finding is that children belonging to the healthy control group showed clear modulation in the angle of eye vergence whereas children in the clinical control group showed weak but significant modulation in the angle of eye vergence (Fig. 2) Children from the ADHD group however showed very weak vergence responses.  Machine-learning models classified ADHD patients from healthy controls with an accuracy >90% and ADHD children from clinical controls with an accuracy of 85%. Thus, in combination with an attention task vergence responses can be used as an objective marker to detect ADHD in children. Similar results were obtained in adult ADHD patients.

 

Alzheimer pilot study

We conducted a pilot study assessing vergence responses in Alzheimer patients, which were divided into three groups. A group with mild cognitive impairment (N=15), another with moderate cognitive impairment (N=15) and the latter with control subjects (N=15). We used an oddball task (Fig. 3) where 80% of the trials had a stimulus in blue whereas the other 20% was in red color. The task was to respond to the red stimuli. The vergence responses differed between the three groups. Healthy subjects showed vergence responses to blue and red stimuli where the ones to red where stronger than the responses to blue stimuli. In patients with mild cognitive impairments the responses to blue stimuli were observed but responses to red stimuli where absent. In moderate cognitive impaired patient no vergence responses were observed.

 

 

Figure 3. Oddbal task (right panel) used in the alzheimer study and vergence responses to frequent blue words (blue traces) and to infrequents red (red traces) stimuli of healthy (upper right panel), mild cognitive impaired (mid right  panel), and  moderate cognitive impaired (lower right panel) subjects.

 

Conclusion

Our observations show that attention related vergence differs between healthy controls and patients with mental disorders. These findings may therefore indicate that the assessment of vergence responses during a cognitive task can be a useful, observer independent tool supporting the clinical diagnosis.