Elsevier

Neurobiology of Aging

Volume 92, August 2020, Pages 28-33
Neurobiology of Aging

Regular article
Cognitive processes in aging effects on attentional alerting

https://doi.org/10.1016/j.neurobiolaging.2020.03.022Get rights and content

Highlights

  • We investigated age-related decline in the ability to use alerting cues.

  • Older adults derived less benefit from visual alerting cues than younger adults.

  • Older adults used auditory alerting cues equally well.

  • Cue spatial predictivity did not impact on aging effects on alerting.

  • Aging effects on alerting may reflect cognitive rather than neuromodulatory changes.

Abstract

Alerting, the process of achieving and maintaining a state of optimal vigilance, is crucial for detecting relevant stimuli and task performance. Age-related decline in the ability to use alerting cues is widely reported and attributed to changes in noradrenergic signaling. However, it remains to be determined whether aging affects all forms of alerting cues equally and whether older adults differently modulate their alerting sensitivity based on differences in cue predictivity relevant to the target task. We examined the performance of 135 younger adults and 103 older adults on three versions of the Attention Networks Test, using locational but spatially nonpredictive visual cues, locational spatially predictive visual cues, and spatially predictive auditory cues. Analysis of alerting effects indicated that while older adults derived less benefit from visual alerting cues than younger adults, they used auditory alerting cues equally well. Furthermore, cue spatial predictivity did not impact on aging effects on alerting. This heterogeneity in aging effects on alerting may indicate that they result primarily from cognitive rather than neuromodulatory changes.

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.

References (49)

  • B.S. Oken et al.

    Vigilance, alertness, or sustained attention: physiological basis and measurement

    Clin. Neurophysiol.

    (2006)
  • I.H. Robertson

    A noradrenergic theory of cognitive reserve: implications for Alzheimer's disease

    Neurobiol. Aging

    (2013)
  • A. Vallesi et al.

    Temporal preparation in aging: a functional MRI study

    Neuropsychologia

    (2009)
  • D. Weinshenker

    Long road to ruin: noradrenergic dysfunction in neurodegenerative disease

    Trends Neurosci.

    (2018)
  • I. Wiegand et al.

    Cue-related processing accounts for age differences in phasic alerting

    Neurobiol. Aging

    (2019)
  • R.S. Williams et al.

    Age differences in the attention network test: evidence from behavior and event-related potentials

    Brain Cogn.

    (2016)
  • S.S. Zhou et al.

    Age-related differences in attentional networks of alerting and executive control in young, middle-aged, and older Chinese adults

    Brain Cogn.

    (2011)
  • A. Zivony et al.

    Multifactorial effects of aging on the orienting of visual attention

    Exp. Gerontol.

    (2019)
  • J. Fan et al.

    The relation of brain oscillations to attentional networks

    J. Neurosci.

    (2007)
  • J. Fan et al.

    Testing the efficiency and independence of attentional networks

    J. Cogn. Neurosci.

    (2002)
  • M.E. Faust et al.

    Individual differences in information-processing rate and amount: implications for group differences in response latency

    Psychol. Bull

    (1999)
  • D. Fernandez-Duque et al.

    Attentional networks in normal aging and Alzheimer's disease

    Neuropsychology

    (2006)
  • E. Festa-Martino et al.

    Interactions between phasic alerting and spatial orienting: effects of normal aging and Alzheimer's disease

    Neuropsychology

    (2004)
  • N. Gamboz et al.

    Age-related differences in the attention network test (ANT)

    Exp. Aging Res.

    (2010)
  • Cited by (4)

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