Regular paperAge-related trends in saccade characteristics among the elderly
Introduction
The proportion of elderly individuals in society is increasing dramatically (Turcotte and Schellenberg, 2006), leading to an increase in the prevalence of age-related neurological disorders that affect the function of the frontal lobes and overall movement control (Gavrilov and Heuveline, 2003). In order to study these disorders most effectively, cognitive deficits due to normal brain changes in healthy aging first need to be understood. The eye movement system is an excellent model to assess brain function (Leigh and Kennard, 2004, Munoz et al., 2007, Ramat et al., 2007). The circuitry controlling saccadic eye movements is well understood and involves areas of the frontal and parietal lobes, basal ganglia, thalamus, visual cortex, superior colliculus, cerebellum, and brainstem reticular formation (Hikosaka et al., 2006, Leigh and Zee, 2006, Moschovakis et al., 1996, Munoz and Everling, 2004, Scudder et al., 2002, Wurtz and Goldberg, 1989). These structures contribute to specific components of saccadic behaviors, and altered saccade performance often gives insight into the etiology of various clinical disorders. Because there is overlap in the frontal cortical areas controlling the production of saccades and the areas involved in controlling various aspects of cognition, measuring saccadic eye movements can provide an important tool to assess cognitive functions subserved by the frontal lobes. These same areas are frequently degenerating as people age (Creasey and Rapoport, 1985, Kramer et al., 2007).
Saccadic eye movement tasks can be designed to probe simple sensory-motor processes as well as higher cognitive functions. Eye movement tasks can be used to dissect different components of the system. In a pro-saccade task, subjects are instructed to look towards an eccentric visual stimulus when it appears. This task has high stimulus-response compatibility and requires a simple, automatic response (Munoz and Everling, 2004). In the anti-saccade task (Hallett, 1978), subjects are instructed to look away from the eccentric stimulus in the opposite direction. The location of the stimulus and the saccade goal are dissociated in this task. Successful completion of the anti-saccade task requires additional stages of processing: suppression of the automatic pro-saccade to the stimulus, followed by voluntary initiation of the anti-saccade away from the stimulus (Munoz and Everling, 2004). The difference between pro- and anti-saccade latencies, the anti-effect, provides a measure of the time it takes for these additional processes. Fixation state can also be manipulated by introducing a gap period between disappearance of the fixation spot and the appearance of the stimulus (Saslow, 1967), which serves to reduce reaction times. A subset of these short-latency stimulus-driven saccades have latencies that approach the minimal afferent and efferent conduction times in the oculomotor system and have been called “express” saccades (for review, see Dorris et al., 1997, Fischer and Weber, 1993). Express saccades have been identified as the first peak in a multimodal distribution of SRTs (Fischer and Boch, 1983, Fischer et al., 1997) and are often reported as minimal or absent in the elderly (Klein et al., 2000, Munoz et al., 1998). Here, we investigate in greater detail the occurrence of these short-latency stimulus-driven saccades in the elderly.
Our knowledge of the neural pathways underlying pro- and anti-saccade generation is under continual debate as new findings emerge. However, studies of patients with frontal lobe lesions (Gaymard et al., 1998, Guitton et al., 1985, Pierrot-Deseilligny et al., 1991, Rivaud et al., 1994) and recent neuroimaging studies of normal individuals (Connolly et al., 2002, Ettinger et al., 2005, Ford et al., 2005, O’Driscoll et al., 1995, Sweeney et al., 1996) have identified specific frontal regions (e.g., dorsolateral prefrontal cortex, frontal and supplementary eye fields) that are involved in voluntary saccade control. For example, lesions to the frontal eye fields (FEF) lead to increased anti-saccade latencies (Gaymard et al., 1998, Rivaud et al., 1994). Lesions to the dorsolateral prefrontal cortex (DLPFC) lead to difficulties in saccade suppression (Gaymard et al., 1998, Guitton et al., 1985, Pierrot-Deseilligny et al., 1991). These lesions do not typically affect pro-saccade generation. Instead, lesions to the posterior parietal cortex and supplementary motor area influence the accuracy and timing of pro-saccade reaction times, respectively (Heide and Kömpf, 1998, Pierrot-Deseilligny et al., 1991). Therefore, contrasting performance on these tasks provides measures of frontal lobe function that can be applied to the elderly.
Numerous studies have described the effects of senescence on saccadic eye movement performance, but their conclusions are inconsistent. Many studies suggest saccade parameters such as reaction times, error rates, and metrics are correlated with aging (Abel and Douglas, 2007, Klein et al., 2000, Munoz et al., 1998, Olincy et al., 1997, Shafiq-Antonacci et al., 1999), whereas others have shown no differences between elderly and younger subjects (Eenshuistra et al., 2004, Pratt et al., 2006). However, there is one broad consensus: the more automatic parameters such as pro-saccades latencies are at best, minimally influenced by aging (Abrams et al., 1998, Kaneko et al., 2004, Munoz et al., 1998, Pratt et al., 2006), whereas more cognitively complex aspects of saccadic performance such as suppression and voluntary initiation of a goal-directed saccade (e.g., anti-saccades) are more strongly influenced by aging (Olincy et al., 1997, Shafiq-Antonacci et al., 1999). This suggests that the neural structures in the oculomotor system responsible for generating pro-saccades such as visual occipital cortex, parietal cortex, the brainstem burst generator, reticular formation, and superior colliculus (Munoz and Everling, 2004) may remain relatively uncompromised as people age compared to structures in the frontal and parietal cortices that are involved in complex cognitive function required in the anti-saccade task (Curtis and D’Esposito, 2003, Pierrot-Deseilligny et al., 2003).
The purpose of this study is to determine the rate at which various saccade parameters change between the ages of 60 and 85 years as assessed with pro- and anti-saccade tasks. If automatic processes are affected by aging, then pro-saccade latencies, and the gap effect, including proportion of express saccades, should be altered. Alternatively, if voluntary processes are primarily affected with aging, then anti-saccade latencies, direction errors, and the anti-effect should be altered. It is hypothesized that performance decrements in the healthy aging will reflect the natural cognitive slowing and cerebral atrophy (Aizenstein et al., 2004, Creasey and Rapoport, 1985, Kramer et al., 2007) that occur over time. Elucidating the patterns of eye movement deficits in aging will help to determine both the feasibility of eye movement testing to evaluate the aging process and the aspects of the saccade system that are most resilient to the aging process.
Section snippets
Subjects
All experimental procedures were reviewed and approved by the Queen's University Human Research Ethics Board. Eighty-one subjects ranging between 60 and 85 years of age were recruited into this study (Table 1). Subjects reported no known visual, neurological or psychiatric symptoms, and had normal or corrected to normal vision. All subjects provided informed consent and were compensated for their participation.
Experimental paradigm
The experiment was conducted in one 40-min session in which subjects performed one
Results
The results of this study can be summarized by four main points: (1) Saccadic reaction times (SRTs) increased with age; (2) intra-subject variability in SRT increased with age; (3) the proportion of direction errors increased with age; and (4) express saccades did not decrease with age (in contrast to previous literature).
Discussion
This study provides a detailed description of the changes in saccade parameters that occur with healthy aging (60–85 years). Saccadic reaction times, intra-subject variability, the range of express saccades, the “anti-effect” (mean latency difference between pro- and anti-saccades), and the proportion of direction errors were all sensitive to the effects of aging. Specifically, the generation of pro-saccades, a simple sensory-motor process, was minimally influenced by age (revealed by
Conclusions
This is the first study to quantify precisely the rate at which saccade control declines across the elderly, and to show that the latency range of express saccades lengthens in the elderly. It appears that aging is selective for specific aspects of the oculomotor circuitry (Shafiq-Antonacci et al., 1999) such that automatic saccade processing declines with age, but at a much slower rate than the voluntary control of saccades. We speculate that the natural neural degeneration that occurs with
Disclosure statement
The authors report no actual or potential conflicts of interest.
Acknowledgements
We would like to thank Irene Armstrong, Don Brien, Brian White, Nadia Alahyane, Rob Marino, and the Munoz Lab for excellent support, technical advice, and editorial comments. We would also like to thank the journal reviewers for their significant effort to make this paper better. This work was supported by the Canadian Institutes of Health Research and the Canada Research Chair Program (DPM).
References (58)
- et al.
Effects of age on latency and error generation in internally mediated saccades
Neurobiol. Aging
(2007) Contrast, probability, and saccadic latency; evidence for independence of detection and decision
Curr. Biol.
(2004)- et al.
Persistent activity in the prefrontal cortex during working memory
Trends Cogn. Sci.
(2003) - et al.
Age-related changes in antisaccade task performance: inhibitory control or working-memory engagement?
Brain Cogn.
(2004) - et al.
Age differences in task switching and response monitoring: evidence from ERPs
Biol. Psychol.
(2007) - et al.
Structural neural correlates of prosaccade and antisaccade eye movements in healthy humans
Neuroimage
(2005) - et al.
The antisaccade: a review of basic research and clinical studies
Neuropsychologia
(1998) - et al.
On the development of voluntary and reflexive components in human saccade generation
Brain Res.
(1997) - et al.
Saccadic eye movements after extremely short reaction times in the monkey
Brain Res.
(1983) Primary and secondary saccades to goals defined by instructions
Vision Res.
(1978)
The microscopic anatomy and physiology of the mammalian saccadic system
Prog. Neurobiol.
Age diminishes performance on an antisaccade eye movement task
Neurobiol. Aging
The spatio-temporal tuning of the mechanisms in the control of saccadic eye movements
Vision Res.
Aging and movement: variability of force pulses for saccadic eye movements
Psychol. Aging
The BOLD hemodynamic response in healthy aging
J. Cogn. Neurosci.
Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus
Exp. Brain Res.
Functional brain imaging of young, nondemented, and demented older adults
J. Cogn. Neurosci.
Human fMRI evidence for the neural correlates of preparatory set
Nat. Neurosci.
The aging human brain
Ann. Neurol.
Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements
J. Neurosci.
Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field
J. Neurosci.
Human express saccades: extremely short reaction times of goal directed eye movements
Exp. Brain Res.
Express saccades and visual attention
Behav. Brain Sci.
Neural processes associated with antisaccade task performance investigated with event-related FMRI
J. Neurophysiol.
Aging of population
Cortical control of saccades
Exp. Brain Res.
Age-related changes in brain activity across the adult lifespan
J. Cogn. Neurosci.
Combined eye-head gaze shifts to visual and auditory targets in humans
Exp. Brain Res.
Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades
Exp. Brain Res.
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