Human eye movements

At the most basic level, human eye movements are vital for survival (Shaikh & Zee, 2018) but

are also pivotal for more complex functions such as social interactions, as these functions are

underpinned by the information acquired during eye movements (Emery, 2000). As humans

separate neural signals (binocular vision) to create a single 3D image with a sensation of depth

(stereopsis). A seminal theory proposed by Hering (1977) suggested that both eyes were

innately mediated by a single neural network and that the left and right eye muscles were

always equally innervated. An opposing theory was proposed by Helmholtz and Atkinson

(1873) who argued that each eye was controlled individually and that there was an element of conscious learning involved in visual orientation. Although both Hering’s and Helmholtz’s

theories hold merit, developments in research techniques have revealed that binocular vision is

a multi-component process, involving at least five neuro-visual systems which originate in the

retina and are distributed throughout the brain (Coubard, 2015). During human visual

processing, both eyes move together several times a second to hold areas of interest on the

fovea (Krauzlis, Goffart & Hafed, 2017). High visual acuity in humans is restricted to the fovea,

a very small pit in the centre of the retina composed of cone photoreceptors (Mccamy, Macknik

& Matinez-Conde, 2014). Eye movements precipitate foveation, the process where areas of

interest within the environment become concentrated on the fovea (Purves et al., 2001). On a

basic level, the decision to move the eyes is dependent upon target-related signals from the

peripheral visual field and signals from the fixated target at the fovea (Krauzlis et al., 2017).

The most studied eye movements in humans are saccades, smooth pursuit and fixations;

discussed below. The control of eye movements is navigated by several subsystems, described

below, and is well-documented in animal and human research.

3.3.1. Saccades

Saccades are high-velocity ballistic movements where both eyes move toward a point of visual

space to redirect the point of fixation (Krauzlis et al., 2017). On average, humans generate a

saccade two to three times per second (Pèlisson, Alahyane, Panouillères & Tilikete, 2010), and

(Berman, Cavanaugh, McAlonan & Wurtz, 2017; Bridgeman, Hendry & Stark, 1975;

Gegenfurtner, 2016).

The saccadic system mediates information about the distance and direction of visual stimuli to

ensure that an area of interest is projected onto the fovea (Sparks, 2002). The system also

controls for gaze errors and integrates information to ensure that the visual scene is perceived

as a unified whole (McCamy et al., 2014). Although all saccades require a degree of attentional

processing, they are generally separated into conscious (voluntary) or unconscious (reflexive)

movements (Ross, Morrone, Goldberg & Burr, 2001; Terao, Fukuda & Hikosaka, 2017).

Reflexive saccades are rapid, automatic eye movements generated in response to a novel

peripheral stimulus, while voluntary saccades are consciously controlled and usually made

based on a symbolic cue or instruction (Walker, Walker, Husain & Kennard, 2000). Evidence

indicates that reflexive and voluntary saccades rely on different neural networks (Cieslik,

Seidler, Laird, Fox & Eickhoff, 2016; McDowell, Dyckman, Austin & Clementz, 2008), but

they also rely on mutual neural networks including; the FEF, DLPFC, PEF, middle temporal

regions, supplementary motor regions, occipital lobes, thalamus, SC, cerebellum, and brain

Figure 22. A diagram to illustrate saccades and fixations during natural vision (reproduced from Rucci & Poletti, 2015, p.500).This image outlines the eye scan pattern of one participant. The yellow lines represent saccades while fixations are represented by the red areas. F1 represents the first fixation, F2 the second fixation and so forth. As demonstrated in the enlarged circle, the eyes continue to elicit small movements during fixations.

3.3.2. Smooth pursuit

Smooth pursuit eye movements are slower than saccades and require continuous rotation of the

eyes to avoid retinal slip (when the amplitude and/or velocity of eye movements are inaccurate,

resulting in a gaze shift that induces the appearance of a stationary item as moving). A retinal

slip would result in a blurring effect and therefore smooth pursuit ensures that moving targets

(e.g. cars, animals, or people) can be tracked with high acuity (Krauzlis et al., 2017; Orban de

Xivry & Lefevre, 2007).

3.3.3. Fixations

In the lapses between saccades and smooth pursuit, the eyes are held relatively still and fixation

defined fixations as ‘microscopic and unnoticed motions of the eyes made when fixating the

gaze between larger eye movements’ (p. 463). It should be noted, while many researchers refer

to fixations as the period when the eyes are stationary, this is somewhat of a misnomer (Rayner,

1998). The eyes are never completely static (Figure 23), and during fixations in humans, there

are three categories of these types of constant eye movements; microsaccades, tremor, and drift

(Martinez-Conde, 2005; see Figure 23).

Figure 23. A diagram to illustrate fixational eye movements (reproduced from Martinez- Conde and Macknik, 2008, p.5). Microsaccades are quick and straight movements, drifts are slow and curved, and tremors are oscillations which overlap drifts.

Fixational eye movements counteract visual neural adaption (adjustment of the sensory system

over time in response to a constant stimulus) so that a stimulus remains visible at fixation. They

also inhibit visual fading (also known as Troxler fading where fixating on one element of the

Figure 24. An example of visual fading in normal vision (reproduced from Martinez- Conde, Macknik & Hubel, 2004, p.231). Precisely fixate on the red dot, without blinking, but pay attention to the light blue circle. After about ten seconds, the blue circle will disappear and it will appear that the red dot is surrounded by white. When you move your fixation the blue circle will reappear.

The human visual system, therefore, presents as a paradox, humans must fixate on an object to

process the finer details but if the fixation is maintained in a strictly static fashion then the

visual scene would fade away. Microsaccades, tremors, and drifts counteract this paradox.

During human visual processing, the most useful visual information is collected during

fixations (Morris, 2015). Human eye fixation data can be analysed to explore saliency in

images or videos owing to the direct association between eye movements and visual attention

(Duc, Bays & Husain, 2008). Distinguishing between areas of interest of a visual scene, as

indicated by fixations, aids the understanding of the behavioural underpinnings of human visual

attention (Atkinson, Simpson & Cole, 2017; Edwards, Stepenson, Dalmaso & Bayliss, 2015).

3.3.3.1. Microsaccades

Microsaccades are small, rapid, straight eye movements which arise during fixations

investigation, although the relationships between microsaccades, perception, and cognition

have been subject to much research over the past decade. Martinez-Conde, et al., (2009)

proposed that regardless of minor discrepancies between research groups, there is a consensus

that microsaccades modulate neural activity in early visual areas through retinal motion.

Microsaccades are reported to enhance edge sensitivity and spatial resolution (Donner &

Hemilä, 2007), and to render latency and contrast in perception (Martinez-Conde et al., 2004).

It is probable that they also play a role in correcting fixation errors (Engbert & Kliegl, 2004).

Also, microsaccades are theorised to be critical in overcoming neural adaption (Costela et al.,

2017; Martinez-Conde, Macknik, Troncoso & Dyar, 2006; Troncoso, Macknik & Martinez-

Conde, 2008), as well as being vital for several other aspects of attention, such as; spatial cueing,

visual exploration, and visual search (Meyberg, Sinn, Engbert & Sommer, 2017; Otero-Millan,

Troncoso, Macknik, Serrano-Pedraza & Martinez-Conde, 2008). Microsaccades and saccades

have similar functional and physical characteristics, implying that both eye movements may

share common oculomotor origins (Otero-Millan et al., 2008; Rolfs, Kliegal & Engbert, 2008).

Animal models and fMRI studies have revealed neuron activation in response to microsaccades

in the LGN, area V1 of the occipital cortex, and extrastriate regions (Donner & Hemilä, 2007;

Peter, Tse, Baumgartner & Greenlee, 2010). Similar to saccades, the SC is thought to be pivotal

for the generation of microsaccades (Chen & Hafed, 2017; Chen, Ignashchenkova, Thier &

Hafed, 2015). Microsaccades and saccades activate burst neurons in the pontomedullary

reticular formation, which is downstream from the SC, and putative motor neurons in the

nearby abducens nucleus (eye motor cranial nerve; Van Gisbergen, Robinson & Gielen, 1981).

3.3.3.2. Tremors

The aperiodic wave-like movement of the eyes is referred to as a tremor and is the smallest of

that the movement may be associated with ensuring there is a continuous source of image

motion to offset visual fading (Martinez-Conde et al., 2004).

3.3.3.3. Drifts

Drifts emerge in synchrony with tremor movements and are slow curved eye movements which

occur during the period's in-between microsaccades (Figure 23). Drifts are hypothesised to

correct fixation position and disparity (Cyr & Fender, 1969; Steinman, Cunitz, Timberlake &

Herman, 1967), and drifts and tremors work in unison during high spatial frequency processing

(Kuang, Poletti, Victor & Rucci, 2012).