Claudia C. Gonzalez

Identifying the causal mechanisms of the quiet eye

Abstract Scientists who have examined the gaze strategies employed by athletes have determined that longer quiet eye (QE) durations (QED) are characteristic of skilled compared to less-skilled performers. However, the cognitive mechanisms of the QE and, specifically, how the QED affects performance are not yet fully understood. We review research that has examined the functional mechanism underlying QE and discuss the neural networks that may be involved. We also highlight the limitations surrounding QE measurement and its definition and propose future research directions to address these shortcomings. Investigations into the behavioural and neural mechanisms of QE will aid the understanding of the perceptual and cognitive processes underlying expert performance and the factors that change as expertise develops.

The brain uses efference copy information to optimise spatial memory.

Does a motor response to a target improve the subsequent recall of the target position or can we simply use peripheral position information to guide an accurate response? We suggest that a motor plan of the hand can be enhanced with actual motor and efference copy feedback (GoGo trials), which is absent in the passive observation of a stimulus (NoGo trials). To investigate this effect during eye and hand coordination movements, we presented stimuli in two formats (memory guided or visually guided) under three modality conditions (eyes only, hands only (with eyes fixated), or eyes and hand together). We found that during coordinated movements, both the eye and hand response times were facilitated when efference feedback of the movement was provided. Furthermore, both eye and hand movements to remembered locations were significantly more accurate in the GoGo than in the NoGo trial types. These results reveal that an efference copy of a motor plan enhances memory for a location that is not only observed in eye movements, but also translated downstream into a hand movement. These results have significant implications on how we plan, code and guide behavioural responses, and how we can optimise accuracy and timing to a given target.

Looking to Learn: The Effects of Visual Guidance on Observational Learning of the Golf Swing

Skilled performers exhibit more efficient gaze patterns than less-skilled counterparts do and they look more frequently at task-relevant regions than at superfluous ones. We examine whether we may guide novices’ gaze towards relevant regions during action observation in order to facilitate their learning of a complex motor skill. In a Pre-test-Post-test examination of changes in their execution of the full golf swing, 21 novices viewed one of three videos at intervention: i) a skilled golfer performing 10 swings (Free Viewing, FV); ii) the same video with transient colour cues superimposed to highlight key features of the setup (Visual Guidance; VG); iii) or a History of Golf video (Control). Participants in the visual guidance group spent significantly more time looking at cued areas than did the other two groups, a phenomenon that persisted after the cues had been removed. Moreover, the visual guidance group improved their swing execution at Post-test and on a Retention test one week later. Our results suggest that visual guidance to cued areas during observational learning of complex motor skills may accelerate acquisition of the skill.

The contribution of the right supra-marginal gyrus to sequence learning in eye movements

We investigated the role of the human right Supra-Marginal Gyrus (SMG) in the generation of learned eye movement sequences. Using MRI-guided transcranial magnetic stimulation (TMS) we disrupted neural activity in the SMG whilst human observers performed saccadic eye movements to multiple presentations of either predictable or random target sequences. For the predictable sequences we observed shorter saccadic latencies from the second presentation of the sequence. However, these anticipatory improvements in performance were significantly reduced when TMS was delivered to the right SMG during the inter-trial retention periods. No deficits were induced when TMS was delivered concurrently with the onset of the target visual stimuli. For the random version of the task, neither delivery of TMS to the SMG during the inter-trial period nor during the presentation of the target visual stimuli produced any deficit in performance that was significantly different from the no-TMS or control conditions. These findings demonstrate that neural activity within the right SMG is causally linked to the ability to perform short latency predictive saccades resulting from sequence learning. We conclude that neural activity in rSMG constitutes an instruction set with spatial and temporal directives that are retained and subsequently released for predictive motor planning and responses.

Cognitive control of saccadic eye movements in children with developmental coordination disorder

The ability to use advance information to prepare and execute a movement requires cognitive control of behaviour (e.g., anticipation and inhibition). Our aim was to explore the integrity of saccadic eye movement control in developmental coordination disorder (DCD) and typically developing (TD) children (8–12 years) and assess how these children plan and inhibit saccadic responses, the principal mechanisms within visual attention control. Eye movements and touch responses were measured (separately and concurrently) in Cued and Non-Cued conditions. We found that children with DCD had similar saccade kinematics to the TD group during saccade initiation. Advance information decreased hand movement duration in both groups during Cued trials, but decrements in accuracy were significantly worse in the DCD group. In addition, children with DCD exhibited greater inhibitory errors and inaccurate fixation during the Cued trials. Thus, children with DCD were reasonably proficient in executing saccades during reflexive (Non-Cued) conditions, but showed deficits in more complex control processes involving prediction and inhibition. These findings have implications for our understanding of motor control in children with DCD.

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI.

The basis of motor learning involves decomposing complete actions into a series of predictive individual components that form the whole. The present fMRI study investigated the areas of the human brain important for oculomotor short-term learning, by using a novel sequence learning paradigm that is equivalent in visual and temporal properties for both saccades and pursuit, enabling more direct comparisons between the oculomotor subsystems. In contrast with previous studies that have implemented a series of discrete ramps to observe predictive behaviour as evidence for learning, we presented a continuous sequence of interlinked components that better represents sequences of actions. We implemented both a classic univariate fMRI analysis, followed by a further multivariate pattern analysis (MVPA) within a priori regions of interest, to investigate oculomotor sequence learning in the brain and to determine whether these mechanisms overlap in pursuit and saccades as part of a higher order learning network. This study has uniquely identified an equivalent frontal-parietal network (dorsolateral prefrontal cortex, frontal eye fields and posterior parietal cortex) in both saccades and pursuit sequence learning. In addition, this is the first study to investigate oculomotor sequence learning during fMRI brain imaging, and makes significant contributions to understanding the role of the dorsal networks in motor learning.

Eye and hand movements during reconstruction of spatial memory

Recent behavioural and biological evidence indicates common mechanisms serving working memory and attention (eg Awh et al, 2006 Neuroscience 139 201–208). This study explored the role of spatial attention and visual search in an adapted Corsi spatial memory task. Eye movements and touch responses were recorded from participants who recalled locations (signalled by colour or shape change) from an array presented either simultaneously or sequentially. The time delay between target presentation and recall (0,5, or 10 s) and the number of locations to be remembered (2–5) were also manipulated. Analysis of the response phase revealed subjects were less accurate (touch data) and fixated longer (eye data) when responding to sequentially presented targets suggesting higher cognitive effort. Fixation duration on target at recall was also influenced by whether spatial location was initially signalled by colour or shape change. Finally, we found that the sequence tasks encouraged longer fixations on the signalled targets than simultaneous viewing during encoding, but no difference was observed during recall. We conclude that the attentional manipulations (colour/shape) mainly affected the eye movement parameters, whereas the memory manipulation (sequential versus simultaneous, number of items) mainly affected the performance of the hand during recall, and thus the latter is more important for ascertaining if an item is remembered or forgotten. In summary, the nature of the stimuli that is used and how it is presented play key roles in determining subject performance and behaviour during spatial memory tasks.

Exploring the quiet eye in archery using field- and laboratory-based tasks

The ‘quiet eye’ (QE)—a period of extended gaze fixation on a target—has been reported in many tasks that require accurate aiming. Longer quiet eye durations (QEDs) are reported in experts compared to non-experts and on successful versus less successful trials. The QE has been extensively studied in the field; however, the cognitive mechanisms underlying the QE are not yet fully understood. We investigated the QEDs of ten expert and ten novice archers in the field and in the laboratory using a computer-based archery task. The computer task consisted of shooting archery targets using a joystick. Random ‘noise’ (visual motion perturbation) was introduced at high and low levels to allow for the controlled examination of the effects of task complexity and processing demands. In this computer task, we also tested an additional group of ten non-archers as controls. In both field and computer tasks, eye movements were measured using electro-oculography. The expert archers exhibited longer QED compared to the novice archers in the field task. In the computer task, the archers again exhibited longer QEDs and were more accurate compared to non-archers. Furthermore, expert archers showed earlier QE onsets and longer QEDs during high noise conditions compared to the novices and non-archers. Our findings show skill-based effects on QED in field conditions and in a novel computer-based archery task, in which online (visual) perturbations modulated experts’ QEDs. These longer QEDs in experts may be used for more efficient programming in which accurate predictions are facilitated by attention control.

Children and Older Adults Exhibit Distinct Sub-Optimal Cost-Benefit Functions when Preparing to Move Their Eyes and Hands

Numerous activities require an individual to respond quickly to the correct stimulus. The provision of advance information allows response priming but heightened responses can cause errors (responding too early or reacting to the wrong stimulus). Thus, a balance is required between the online cognitive mechanisms (inhibitory and anticipatory) used to prepare and execute a motor response at the appropriate time. We investigated the use of advance information in 71 participants across four different age groups: (i) children, (ii) young adults, (iii) middle-aged adults, and (iv) older adults. We implemented ‘cued’ and ‘non-cued’ conditions to assess age-related changes in saccadic and touch responses to targets in three movement conditions: (a) Eyes only; (b) Hands only; (c) Eyes and Hand. Children made less saccade errors compared to young adults, but they also exhibited longer response times in cued versus non-cued conditions. In contrast, older adults showed faster responses in cued conditions but exhibited more errors. The results indicate that young adults (18–25 years) achieve an optimal balance between anticipation and execution. In contrast, children show benefits (few errors) and costs (slow responses) of good inhibition when preparing a motor response based on advance information; whilst older adults show the benefits and costs associated with a prospective response strategy (i.e., good anticipation).

Using MVPA to decipher neural correlates of visual sequence learning in the brain.

Using top-down memory-driven information to guide actions is the common method for successful and efficient completion of most everyday activities. Many previous studies have demonstrated a role of the frontal and parietal cortices in top-down processing with a number of studies revealing attentional modulations and maintenance of neuronal activity during delays in these areas. These areas have been extensively studied in regards to explicit visual working mechanisms, but its role for motor learning is currently unclear. We have implemented a novel and equivalent saccade and pursuit sequence-learning paradigm inside an fMRI scanner to investigate how early motor learning is implemented in the brain and more specifically within this fronto-parietal network. To achieve this we used a multivariate analysis approach (MVPA) to a priori regions of interest (prefrontal, frontal and parietal cortices) to evaluate how patterns of activation within these areas change with increasing repetition i.e. during visuomotor learning. The results revealed patterns of activity within these areas that reflect early motor learning that is analogous to the dorsal attentional network, indicating an overlap in function for the fronto-parietal network in attention, working memory and early motor learning. Meeting abstract presented at VSS 2015.