Regular articleCognitive processes in aging effects on attentional alerting
Introduction
It has long been recognized that attention is not a single cognitive entity, but rather a family of processes and brain networks that modulate perception to achieve effective functioning in the world (Posner and Peterson, 1990). One key attentional process is alerting, defined as achieving and maintaining a state of optimal vigilance for detecting relevant stimuli and task performance (Fan et al., 2003, Oken et al., 2006). The process of alerting is expressed in changes in heart rate and brain oscillatory activity related to inhibiting competing activities (Kahneman, 1973, Oken et al., 2006). The brain's alerting system is associated with cortical distribution of norepinephrine (NE) and involves thalamic, frontal, and parietal brain regions (Coull et al., 1996, Marrocco et al., 1994, Raz and Buhle, 2006). A common paradigm for testing alerting involves the provision of a temporal warning signal prior to the appearance of a target. Such cues initiate a change in phasic alertness, by replacing the current resting state with a state of preparation for stimulus detection (Posner and Petersen, 1990). This is distinguished from tonic alertness, the sustained level of preparedness over a longer period of time (Sturm and Willmes, 2001).
As we have noted in our recent review of attentional orienting in aging (Erel and Levy, 2016), age-related decline in alerting is a somewhat consistent finding, both in studies testing alerting alone (Gola et al., 2012) and in studies testing alerting together with orienting and executive attention using Posner and colleagues' Attention Networks Test (ANT) paradigm. Although earlier studies suggested that this aspect of attention is generally preserved (Rabbitt, 1984, Talland and Cairnie, 1961) or even improved (Fernandez-Duque and Black, 2006) in older adults, there is cumulative data indicating reduced alerting abilities in aging (e.g., Festa-Martino et al., 2004, Gamboz et al., 2010, Jennings et al., 2007, Zhou et al., 2011). Recent cueing paradigms that control for confounds such as general slowing (Salthouse, 1996), cue repetitiveness, cue duration, and lack of temporal uncertainty within blocks (Festa-Martino et al., 2004, Jennings et al., 2007) indicate age-related decline in alerting, as expressed in speeded task responding (Zhou et al., 2011). The diminished alerting effect in aging has been attributed to diminished attentional resources (Mahoney et al., 2010, Tun et al., 2009) possibly due to a decline in cortical levels of NE (Ferrari and Magri, 2008, Lohr and Jeste, 1988, Robertson, 2013).
While alerting is asserted to be orthogonal to other aspects of attention (e.g., Ishigami et al., 2016), it is possible that the effect of aging on alerting is sensitive to parameters relevant to orienting, such as the format of attentional cues, and to their overall predictive character. Specifically, we may ask: do visual and auditory alerting cues equally benefit (or fail to benefit) older adults' visual discrimination performance? Are age-related changes in phasic alerting affected by whether the cues are beneficially predictive of subsequent target location (which determines their orienting value)? It is possible that if cues are unreliable in their spatial predictivity when that is relevant to efficient task performance, they will become ignored as temporal predictors as well. The way younger and older adults relate to such spatially nonpredictive cues may differ. Dependence of the impact of aging on alerting on cue format, or on spatial orienting value, would indicate that such age-related changes in alerting might not be monolithically determined by factors such as NE levels, but rather result from complex cognitive processes.
We have recently collected data on the performance of older and younger adults on three versions of the ANT, using (1) locational but spatially nonpredictive visual cues, (2) locational spatially predictive visual cues, and (3) spatially predictive auditory cues. Facets of those data relating to orienting functions, but not to alerting, were reported in Zivony et al. (2019a; in press). In the current study, we use those data to examine whether cue visual or auditory manifestation and their predictivity modulate the impact of aging on alerting.
Section snippets
The Attention Networks Test
The analyses reported below were carried out on an extensive data set tracking attentional performance in 103 older adults and 135 younger adults (participant details provided below). That data set was collected from three versions of the ANT paradigm in a between-subjects design. This test format, requiring discrimination between types of visual target stimuli that may appear in a validly cued, invalidly cued, or uncued spatial location, enables simultaneous assessment of the alerting,
Results
To examine whether aging affects alerting, we entered Z-transformed RTs and accuracy rates as dependent measures in ANOVAs with age group (young adult vs. old adult) and cue format (locational non-predictive, locational predictive, symbolic predictive) as between-subject variables and with cue condition (double cue vs. absent cue) as a within-subject condition (see Fig. 2).
Discussion
As in many prior studies, we observed that older adults benefit less than young adults from a brief visual alerting signal (Festa-Martino et al., 2004, Gamboz et al., 2010, Gola et al., 2012, Jennings et al., 2007, Zhou et al., 2011). However, unlike previous studies, we also examined alerting effects in response to spatially uninformative auditory cues, and found no age differences in alerting to such cues. This cue was composed of the words “up” and “down” overlaid on one another. Therefore,
CRediT authorship contribution statement
Hadas Erel: Methodology, Software, Investigation, Project administration. Alon Zivony: Formal analysis, Writing - original draft. Daniel A. Levy: Conceptualization, Methodology, Writing - original draft, Supervision, Funding acquisition.
Acknowledgements
This study was supported by grant no. 3-9542 from the Chief Scientist Office, Ministry of Health, Israel, to DAL. We thank Prof. Mara Mather and one additional reviewer for insightful beneficial suggestions. The authors have no competing interests to declare.
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