Elsevier

Brain Research

Volume 1469, 21 August 2012, Pages 24-34
Brain Research

Research Report
Keeping focused: Sustained spatial selective visual attention is maintained in healthy old age

https://doi.org/10.1016/j.brainres.2012.06.019Get rights and content

Abstract

A better understanding of age-related change in the attentional modulation of perceptual processing may help elucidate cognitive change. For example, increased cognitive interference due to inappropriate processing of irrelevant information has been suggested to contribute to cognitive decline. However, it is not yet clear whether interference effects observed at later stages, such as executive function or response selection, are caused by leaky attentional selection at early, sensory stages of processing. Here, we investigated attentional control of sensory selection by comparing younger and older adults' ability to sustain spatial selective attention to one of two centrally presented, overlapping rapid serial visual presentation (RSVP) letter sequences, one large and one small. These stimuli elicited separable steady-state visual evoked potentials (SSVEP), which provide an index of early visual processing for each stimulus separately and are known to be modulated by selective attention. The condition of most interest required participants to attend to the larger letters while ignoring the smaller letters, as these foveally presented irrelevant stimuli were expected to present the strongest interference. Although the rapid presentation rates made the task demanding, detection ability did not differ between young and older adults. Accordingly, attentional modulation of SSVEP amplitudes was found in both age groups. Neither the magnitude nor the cortical sources of these SSVEP attention effects differed between age groups. Our results thus suggest that in the current task, the effect of voluntary spatial attention on sustained sensory processing in early visual areas is maintained in healthy old age.

Highlights

► Leaky attentional selection at early sensory stages of processing may contribute to cognitive change in old age. ► We tested integrity of sensory selection in a sustained task using SSVEP to measure attentional modulation of visual processing. ► No effect of age found in accuracy or SSVEP, suggesting sustained spatial selection is maintained in healthy old age.

Introduction

Understanding the cognitive changes that occur naturally as we age has become of increasing importance (Brayne, 2007) and cognitive ageing research has converged on causal factors that might explain decline in executive function in old age (Rozas et al., 2008). One such factor is interference from irrelevant information, best exemplified by the inhibitory deficit hypothesis (Lustig et al., 2007), which explains age-related cognitive decline in terms of a failure to appropriately limit selection to relevant information only. In line with this theory, many studies have found that older adults show more interference from distractors than their younger counterparts (see Guerreiro et al., 2010 for a comprehensive review). Evidence has however been mixed—although many studies have shown a strong effect of age (e.g. de Fockert et al., 2009, Gazzaley et al., 2005, Waszak et al., 2010) others have reported no greater distraction or interference effects (e.g. Lorenzo-López et al., 2008, Verhaeghen and Cerella, 2002, Wild-Wall et al., 2008). Failures in selection may occur at multiple stages of processing and here we aimed to clarify whether older adults exhibit a general deficit at the earliest stage of selection—namely attentional control of sensory processing. Leaky sensory selection mechanisms may have important consequences for later cognitive processing, so a better understanding of age-related changes in the sensory effects of visual selective attention is of great importance both for attentional ageing research and for a clearer understanding of cognitive decline.

Although visual attention in older adults has been a topic of interest for some time (for reviews, see Groth and Allen, 2000, Kramer and Madden, 2008), few studies have directly investigated age-related change in the effects of attention on sensory processing. It is indeed difficult to draw conclusions about the locus of a deficit when only behavioural measures are examined. Obtained age effects may be due to deficits at post-sensory processing stages, or, on the other hand, sensory interference may be compensated for at later stages and thus masked at the level of behaviour. Fortunately, visual attention research provides established psychophysiological methods for examining the effects of top-down attentional selection on sensory cortical responses as well as a clear description of the sensory effects that can be expected in younger adults (reviewed in Carrasco, 2011). In order to gauge these effects, selective attention tasks typically require participants to attend to a subset (defined spatially or by feature) of multiple, transiently presented stimuli (see Hillyard et al., 1998 for a review). Three recent studies investigating age-related change (de Fockert et al., 2009, Quigley et al., 2010, Schmitz et al., 2010) have together provided strong evidence for older adults' difficulty in preventing the visual processing of task-irrelevant information. However, it is important to look at the details of each experiment before generalising their findings. As in many studies, the first of these experiments (de Fockert et al., 2009) used transient presentation of stimuli. Analysis of an early component of the event-related potential (ERP) clearly showed inappropriate processing of distractors in the older group only, but it is possible that these results reflect a delayed onset rather than an absence of the sensory effects of attentional selection. Along these lines, evidence for a slowed onset of attentional effects has been found in a series of experiments investigating the role of selective attention in working memory (Gazzaley et al., 2005, Gazzaley et al., 2008, Zanto et al., 2010). Thus, it is important to consider the timing involved before drawing general conclusions about attentional decline. The other two studies (Quigley et al., 2010, Schmitz et al., 2010) used longer presentation durations and analysis intervals but involved presentation of overlapping stimuli, meaning that these tasks could not be solved using spatial selection. As such, it is not yet clear whether previously reported age-related differences in sensory selection during simultaneous stimulus presentation represent a general deficit, or whether these findings are limited to situations involving transient stimuli and/or non-spatial attentional selection. The current experiment provides a first step towards clarifying this issue by investigating spatial selection of continuously presented stimuli.

Directly assessing the processing of each individual stimulus in a multi-stimulus display with macroscopic measures of brain activity is inherently difficult. As a consequence, existing selective attention studies with older adults have only been able to indirectly map stimulus processing to individual stimuli. For example, the above-mentioned studies used a face-sensitive ERP component (de Fockert et al., 2009) and fMRI adaptation in visual association areas that preferentially respond to members of particular stimulus categories (Schmitz et al., 2010). Here we used the electroencephalogram (EEG) to measure steady-state visual evoked potentials (SSVEP), which allow direct assessment of the effect of attentional selection on on-going sensory processing in early visual areas of the human brain (see Andersen et al., 2011b for a recent review). Temporally regular sensory input, for example a flickering visual stimulus, leads to a regular cortical response that oscillates at the stimulation frequency and is not subject to habituation over time (Regan, 1966). This steady-state response is ideally suited to attention research–attention to a stimulus has been shown to robustly lead to an—increase in amplitude of the corresponding SSVEP response (Morgan et al., 1996, Müller and Hillyard, 2000), and simultaneous presentation of frequency-tagged stimuli allows comparison of the individual cortical responses to each stimulus under different attentional conditions (e.g. Andersen et al., 2008, Müller et al., 2003, Toffanin et al., 2009). Importantly, the SSVEP reflects sustained visual responses rather than the brief responses to event onsets captured by the ERP. It has been shown that attention can differentially affect the two (Andersen et al., 2011a, Müller and Hillyard, 2000) and this is extremely useful in disentangling delayed attention effects from absent effects. If older adults simply cannot use selective attention to modulate sensory processing, then the age effects found for attentional modulation of early ERP components (e.g. de Fockert et al., 2009) should also be evident in the sustained response captured by the SSVEP. If, on the other hand, the sensory effects of selective attention are delayed in time in older adults (e.g. Gazzaley et al., 2008), then we would expect to find significant effects of attention on the SSVEP for both age groups.

Here, we instructed young and older participants to attend to one of two simultaneously presented rapid serial visual presentation (RSVP) letter sequences, which were both centrally presented but differed in size (see Fig. 1), and to respond to occurrences of a target letter in the attended stream only. Both letter sequences updated at different rates, which elicited distinguishable SSVEP responses. The task was adapted from an experiment which demonstrated that the spatial focus of attention is not limited to a simple ‘spotlight’, but can also be deployed in an annulus—the processing of large stimuli extending into the periphery can be enhanced without a concomitant enhancement in the processing of centrally located stimuli (Müller and Hübner, 2002). This stimulus configuration is particularly well suited for investigating age differences in the effects of selective attention on sensory processing for several reasons. First, a series of behavioural studies has shown that distractors centred at fixation produce larger interference effects than distractors in the periphery, due to “preferential access to attention” (Beck and Lavie, 2005). In conditions requiring attention to the large surrounding letters, subjects need to ignore the foveally presented, task-irrelevant small letters. If older adults have difficulty in appropriately controlling sensory selection of irrelevant information, this should thus be particularly evident when the large letters are attended. Second, the results of the earlier experiment with young subjects revealed that the size of letters attended and speed of RSVP update have an effect on task difficulty (Müller and Hübner, 2002), so the four conditions of the experiment allow a sensitive comparison of behavioural performance under varying task demands. Third, both stimuli are centred at and do not extend far from fixation, so we can be sure that they fall within older participants' reduced visual field (cf. Haegerstrom-Portnoy et al., 1999). One might argue that the spatial selection involved might be mediated by a broadening/narrowing of focus and thus differs from the shifts in location traditionally employed in spatial attention studies. However, the results of the previous study suggested that stimulus selection was not realised by changes in the extent of the attentional focus, but rather by spatially attending or ignoring the respective letter stream. Thus, this task provides a means of investigating age-related differences in the sensory consequences of sustained spatial selective attention under conditions of varying interference.

In summary, the study of age-related changes in attentional control of sensory processing is under-explored, although it is of great importance to better understand change in other, more cognitive domains such as working memory or executive control. The current EEG study investigated age-related change in sustained spatial selection among continuously and simultaneously presented visual stimuli and addressed two questions in particular. First, we wanted to know whether older adults are equally capable of performing tasks requiring sustained selective spatial attention—an issue that has, to our knowledge, not yet been explored. Second, we investigated the modulation by sustained selective attention of cortical processing in early visual areas by measuring the effect of attention on the amplitude of SSVEP responses and localising the sources of these effects in cortex. These questions have important implications for theories of cognitive ageing such as the inhibitory deficit hypothesis—if an age-related difference were to be found here under sustained attention conditions, this would strongly support a deficit in spatial attentional control at the level of sensory processing rather than a delay in onset. Indeed, coupled with recent results from non-spatial tasks (Quigley et al., 2010, Schmitz et al., 2010), this would suggest a general age-related decline in early attentional selection.

Section snippets

Behavioural results

Hits and false alarms were defined as button presses occurring between 300 and 1000 ms after the appearance of the letter H in the attended and unattended stimulus, respectively. Participants' ability to discriminate between targets and distractors was quantified by the sensitivity index d′, and their internal response threshold was estimated by the response bias C. d′ and C were calculated from the hit and false alarm rates (Wickens, 2001) for each experimental condition and then averaged over

Discussion

Two main questions of interest were investigated here: first, whether older adults have difficulties ignoring irrelevant information during sustained selective visual attention, and second, whether the effects of spatial selection on sustained sensory responses are subject to age-related change. These are addressed in detail below. We expected to see the strongest evidence for an age difference, if present, in behavioural performance and SSVEP amplitude in conditions requiring target detection

Subjects

Younger subjects were recruited by advertisement at the University of Leipzig, and older subjects by advertisement in the University of Leipzig's Seniors' College, which offers short series of lectures to members of the public. Older subjects were pre-screened by telephone interview to be clear of history of neurological illness, ophthalmologic problems, and medications affecting the central nervous system. In addition, all subjects completed the mini-mental state examination (Folstein et al.,

Acknowledgments

We thank Renate Zahn for assistance in data acquisition and Alper Açık and Björn Herrmann for helpful comments on an earlier version of the manuscript. Research was supported by the Deutsche Forschungsgemeinschaft, graduate programme “Function of Attention in Cognition”.

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