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A Probe Into the Dorsolateral Prefrontal Cortex in Alzheimer's Journal of Alzheimer’s Disease 19 (2010) 781–793 781 DOI 10.3233/JAD-2010-1275 IOS Press Review Article Antisaccades: A Probe into the Dorsolateral Prefrontal Cortex in Alzheimer’s Disease. A Critical Review Liam D. Kaufmana,b,∗, Jay Prattc, Brian Levinec,d and Sandra E. Blacka,b,d aLC Campbell Cognitive Research Unit, Division of Neurology, Deparatment of Medicine, Sunnybrook Research Institute, Sunnybrook Health Sciences Centre, University of Toronto Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada bInstitute of Medical Science, University of Toronto, Toronto, Ontario, Canada cDepartment of Psychology University of Toronto, Toronto, Ontario, Canada dThe Rotman Research Institute, Toronto, Ontario, Canada Accepted 17 September 2009 Abstract. The number of people living with Alzheimer’s disease (AD), the major cause of dementia, is projected to increase dramatically over the next few decades, making the search for treatments and tools to measure the progression of AD increasingly urgent. The antisaccade task, a hands- and language-free measure of inhibitory control, has been utilized in AD as a potential diagnostic test. While antisaccades do not appear to differentiate AD from healthy aging better than measures of episodic memory, they may still be beneficial. Specifically, antisaccades may provide not only a functional index of the Dorsolateral Prefrontal Cortex (DLPFC), which is damaged in the later stages of AD, but also a tool for monitoring the progression of AD. Further work is required to: 1) strengthen the link between antisaccade errors, in AD, with the DLPFC; 2) insure that antisaccade errors do not result from memory, visuospatial, or other deficits associated with AD; and 3) further validate the clinical analogue of the antisaccade task. Keywords: Alzheimer’s disease, antisaccades, dementia, dorsolateral prefrontal cortex INTRODUCTION rope, while in Asia it will nearly quadruple [1]. As new pharmaceuticals are developed to treat and possi- Alzheimer’s disease (AD), characterized by gradual, bly prevent AD, early diagnosis and disease treatment progressive loss of episodic memory, is the most com- monitoring will become increasingly important. Cur- mon single cause of dementia affecting four million rently used NINCDS-ADRDA diagnostic criteria and Americans and is quickly becoming one of the “most the newly proposed criteria [2] both include deficits burdensome health conditions worldwide” [1]. In the in episodic memory as the core diagnostic feature of next two decades, the number of individuals diagnosed AD. Although decline in episodic memory is central with AD will nearly double in North America and Eu- to typical AD, an understanding of additional deficits associated with AD may aid in tracking the progression ∗Correspondence to: Liam D. Kaufman, LC Campbell Cognitive of AD and monitoring the effectiveness of treatments. Research Unit, Division of Neurology, Dept. of Medicine, Sunny- Once such deficit that has been noted in patients with brook Research Institute, Sunnybrook Health Sciences Centre, Uni- AD is difficulty exerting flexible control over prepotent versity of Toronto, Room A421- 2075 Bayview Avenue, Toronto, Ontario, M4N 3M5, Canada. Tel.: +1 416 480 4551; Fax: +1 416 saccades during the antisaccade task (Table 1) [3–10]. 480 4552; E-mail: [email protected]. Results from antisaccade studies indicate that the task ISSN 1387-2877/10/$27.50 2010 – IOS Press and the authors. All rights reserved 782 L.D. Kaufman et al. / Antisaccades: A Probe into the Dorsolateral Prefrontal Cortex in Alzheimer’s Disease may have potential for monitoring progression, specif- direction than adults [13,14]. Between the ages of 10 ically the emergence of dorsofrontal functional deficits and 15, antisaccade performance improves dramatical- in AD, as well as monitoring new treatments. ly and continues to improve into early adulthood. The reduction in antisaccade error rates appears to close- ly mirror structural changes that occur from childhood THE ANTISACCADE TASK to adulthood. For example, volumetric imaging has shown that between the ages of 8 and 22, total white In the antisaccade task, a participant is told to inhibit matter volume increases linearly with age [15]. In the a reflexive (or automatic), visually-guided saccade to frontal lobes, grey matter shows a non-linear increase a peripheral target, and to make an antisaccade in the over time, with a peak volume around the age of 12, opposite direction to a non-existent target (Fig. 1) [11]. followed by a gradual decline presumed to relate to Thus, the antisaccade task probes one’s ability to exert synaptic extermination [15]. In addition to volumet- flexible control by overcoming the prepotent reflexive ric indices of structure, diffusion tensor imaging (DTI) saccade response. If the participant fails to inhibit the has revealed that fractional anisotropy, a measure of reflexive saccade and makes a saccade towards the pe- white matter microstructural integrity and myelination, ripheral target, this constitutes an antisaccade (i.e., in- increases in the frontal lobes from childhood to adult- hibition) error. The task has been widely adopted in hood [16]. some clinical disorders because of several advantages During older adulthood, aging is associated with a over other cognitive tests: it does not require a verbal general decline in grey matter volume [17] and a reduc- or manual response and is well tolerated in patients tion in white matter fractional anisotropy [18]: a grad- with dementia, including AD, and frontotemporal de- ual reversal of developmental changes. Studies of an- generation (FTD) [8]. Furthermore, patients are often tisaccade performance from young adulthood onwards unaware of their mistakes and rarely, if ever, become have reported either a non-significant upward trend in frustrated. Although the task relies on making a par- error rates [4,7,12,19] or a significant increase in error simonious response – a saccade –, multiple and easily rates with aging [13,20,21]. Furthermore, fMRI has quantifiable metrics, such as corrected versus uncor- revealed a compensatory shift in antisaccade related ac- rected errors, saccade amplitudes, and latencies, can be tivation between young adults and older adults indica- derived from the task. tive of functional differences between young and older Recently, the neural correlates of the task have be- adults [19]. come better understood [12]. An absence of verbal or manual responses enables the antisaccade task to be used in neuroimaging environments, such as mag- FUNCTIONAL IMAGING STUDIES netoencephelography (MEG) and functional magnet- ic resonance imaging (fMRI), which do not tolerate Developmental and aging studies indicate a relation- movement well. Consequently non-human primates ship between frontal lobe function and inhibitory fail- can be studied using the antisaccade task, providing a ure in the antisaccade task. Functional neuroimag- model for understanding its neural correlates [12]. The ing techniques such as positron emission tomography relative simplicity of the antisaccade task has enabled (PET) and fMRI have provided more specific infor- children, adolescents, adults, and the elderly to com- mation on neural substrates, implicating specific re- plete the task, which has also provided developmental gions within the frontal lobes for successful antisac- data [13]. cade generation. In the simplest imaging experiments using either PET or fMRI, blocks of antisaccades were compared to prosaccades, and revealed greater activa- DEVELOPMENTAL CHANGES tion for antisaccades in the frontal eye fields and the superior parietal lobule, when compared with prosac- The frontal lobes undergo rapid changes from child- cades [22,23]. Early functional imaging studies led to hood to adolescence, followed by gradual changes dur- conflicting views on the involvement of the dorsolat- ing later adulthood as the later evolved structures such eral prefrontal cortex (DLPFC): some found activation as the frontal lobes gradually become fully myelinated. in the right DLPFC [24,25], while others did not [22, Children under 10 years of age have great difficulty 26]. However, block designs have many shortcomings performing the antisaccade task, making more errors in for analyzing antisaccade related activity. Block de- L.D. Kaufman et al. / Antisaccades: A Probe into the Dorsolateral Prefrontal Cortex in Alzheimer’s Disease 783 signs do not allow temporal differentiation between the by Stuss and Alexander [31], task setting and task mon- components of an antisaccade such as: 1) inhibiting a itoring. The antisaccade task requires greater task-set prosaccade; 2) generating an antisaccade; and 3) mak- demands than the prosaccade task, which may explain ing a retrosaccade back to the central fixation. There is the greater left DLPFC activation for antisaccades rel- the potential that activation could either be nullified or ative to prosaccades. In contrast to task setting, involv- enhanced by a negative or a positive response respec- ing the left DLPFC, Stuss and Alexander [31] report- tively, from one of the other components. Furthermore ed an association between damage of the right lateral it is difficult to tease apart the effect of antisaccade di- dorsalfrontal regions and impairments in task monitor- rectional errors, reduced latencies, and hypometric re- ing. Greater right DLPFC activation for correct an- sponses on the blood oxygen level dependent (BOLD) tisaccades, relative to incorrect antisaccades, may re- signal. Event-related
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