Elsevier

Neuropsychologia

Volume 50, Issue 7, June 2012, Pages 1502-1513
Neuropsychologia

Age-related loss in attention-based modulation of tactile stimuli at early stages of somatosensory processing

https://doi.org/10.1016/j.neuropsychologia.2012.03.002Get rights and content

Abstract

Normal aging has been linked to impairments in gating of irrelevant sensory information and neural markers of diminished cognitive processing. Whilst much of the research in this area has focussed on visual and auditory modalities it is unclear to what degree these findings apply to somatosensation. Therefore we investigated how age impacts early event-related potentials (ERPs) arising from relevant or irrelevant vibrotactile stimuli to the fingertips. Specifically, we hypothesised that older adults would demonstrate reduced attention-based modulation of tactile ERPs generated at early stages of cortical somatosensory processing. In accord with previous research we also expected to observe diminished P300 responses to attended targets and behavioural deficits. Participants received vibrotactile stimulation to the second and fifth digit on the left hand and reported target stimuli on one digit only (as instructed) with comparisons between two age groups: (1) Young adults (age range 20–39) and (2) Older adults (age range 62–89). ERP amplitudes for the P50, N70, P100, N140 and long latency positivity (LLP) were quantified for attended and non-attended trials at several electrodes (C4, CP4, CP3 and FC4). The P300 in response to attended target stimuli was measured at CPZ. There was no effect of attention on the P50 and N70 however the P100, N140 and LLP were modulated with attention. In both age groups the P100 and LLP were more positive during trials where the stimuli were attended to, whilst the N140 was enhanced for non-attended stimuli. Comparisons between groups revealed a reduction in P100 attention-based modulation for the older adults versus the young adults. This effect was due to a loss of suppression of the non-attended stimuli in older subjects. Moreover, the P300 was both slower and reduced in peak amplitude for older subjects in response to attended targets. Finally, older adults demonstrated impaired performance in terms of both reduced target detection accuracy and in reporting more false positives. Overall, present results reveal a deficit in suppressing irrelevant tactile information during an attention-demanding task which possibly relates to reduced markers of performance. Such a loss of inhibitory function is consistent with age-related change associated with a decline in executive control via prefrontal regions.

Highlights

► Attention-based modulation of tactile signals from the hand diminished in older adults. ► This loss was evident at early cortical stages of somatosensory processing. ► As expected, the P300 was slower and smaller in older vs. younger subjects. ► Age was associated with increased errors during tactile target discrimination.

Introduction

Progressive cognitive decline, indexed by decreased performance on memory and attention-related tasks is one of the major changes an individual will endure with age. Many researchers have worked to establish the neural mechanisms which bring about age-related cognitive impairment (Drag and Bieliauskas, 2010, Gazzaley and D’Esposito, 2007, MacDonald et al., 2009, Reuter-Lorenz and Park, 2010). Consequently, a number of models have been advanced to explain degraded performance. Traditional models include a general slowing of processing speed, an inability to inhibit irrelevant distractive information, and a deterioration of top-down regulation via prefrontal regions (Dempster, 1992, Hasher and Zacks, 1988, Salthouse, 1996, West, 1996). Importantly, these accounts are not mutually exclusive and the contemporary view acknowledges that age-related cognitive decline stems from a complex interplay of factors.

A key to optimal cognitive function is the ability to maintain relevant data in working memory whilst preventing interference from irrelevant sources of information. A number of studies have demonstrated age-related deficits in this regard. In fact, it appears that the main disparity between young and older adults is not so much an inability to attend to task-relevant information but in a compromised ability to suppress task-irrelevant information (Reuter-Lorenz & Park, 2010). This has also been discussed by some authors in terms of increasing levels of noise in the aging brain (MacDonald et al., 2009). Any impaired filtering may result in a greater propensity to overwhelm neural processing networks (Awh and Vogel, 2008, McNab and Klingberg, 2008); networks such as prefrontal areas which already exhibit a lower ceiling of activation in older adults during working memory tasks (Reuter-Lorenz & Park, 2010).

An area which is critical in providing resistance to distraction is the prefrontal cortex (PFC) (Knight, Staines, Swick, & Chao, 1999). Numerous lines of evidence including animal models of selective attention (Artchakov et al., 2009, Bartus and Levere, 1977), lesion studies in humans (Chao and Knight, 1995, Chao and Knight, 1998) and imaging work (Dolcos, Miller, Kragel, Jha, & McCarthy, 2007) have established clear links between prefrontal activity, suppression of distracters and subsequent cognitive performance. Indeed, PFC acts to suppress irrelevant information early in the processing stream, including at the earliest cortical stages of sensory processing and even at the thalamus prior to cortical entry (Cao et al., 2008, Yamaguchi and Knight, 1990, Yingling and Skinner, 1976, Zikopoulos and Barbas, 2006). Given the established role of PFC in task-related gating and cognitive performance it is essential to note that this region undergoes disproportionately greater deterioration with age compared with other brain structures (Jernigan et al., 2001, Raz et al., 1997, Resnick et al., 2003). Thus the loss of inhibitory interference control in older adults may originate at least partly from diminished prefrontal function.

Much of the research on age-related cognitive processing has emphasised visual or auditory modalities with comparably little focus on somatosensation. Whilst there are likely many similarities in how age impacts cognitive performance driven by various sensory systems, important differences in how aging impacts visual and auditory processes have already been noted (Ceponiene, Westerfield, Torki, & Townsend, 2008). Consequently a focus on somatosensation is warranted to develop a more complete model of neurological changes associated with age. The main purpose of the current study was to investigate age-related changes in somatosensory gating during a tactile discrimination task. Furthermore, we wished to explore how these changes may relate to recent findings in our lab where transient suppression of the dorsolateral prefrontal cortex (DLPFC) was used to investigate the role of this region in attention-based sensory gating (Bolton & Staines, 2011). In our previous study, subjects performed a within-hand vibrotactile discrimination task where they were required to attend to targets on one digit, whilst ignoring distracter targets on another digit. Following the application of continuous theta burst stimulation over DLPFC, subjects demonstrated a loss of attention-based modulation over tactile evoked-potentials that were reflective of uni-modal somatosensory processing. These results supported the view that prefrontal areas regulate somatosensory signal transmission at an early cortical processing stage based upon task-relevance. Given that one explanation for age-related cognitive decline involves selective deterioration of prefrontal areas (e.g. loss of cortical volume or abnormalities in white matter), comparisons between the DLPFC-inhibited group with older adults could offer insight into the role of deficient frontal control in driving age-linked deficits, particularly in the context of somatosensory gating.

Electroencephalography (EEG) has been useful in studies on aging to reveal delayed processing of sensory information and in exposing a selective loss in suppressing distracters as they pass through various cortical centres (Dustman, Shearer, & Emmerson, 1993). In particular, event-related potentials (ERPs) following somatosensory stimulation (either electrical or mechanical) provide a useful probe into cortical processing of somatosensory information. The ensuing ERP profile offers a means of investigating both early sensory processing such as the P50 or P100 components which reflect unimodal somatosensory generators (Allison et al., 1991, Hamalainen et al., 1990), and/or later more endogenous markers such as the N140 or target-elicited P300 (Brazdil et al., 1999, Hamalainen et al., 1990, Linden, 2005). Given the sensitivity of somatosensory ERP measures to attentional manipulation (Adler et al., 2009, Bolton and Staines, 2011, Eimer and Forster, 2003, Gillmeister et al., 2010, Iguchi et al., 2005), they provide an ideal means of exploring age-related changes in signal processing. To date, a thorough investigation into age-related changes in attention-based modulation of somatosensory information has not been undertaken.

The present study explored the impact of age on spatial attention to tactile information at early cortical stages of somatosensory processing. Using a vibrotactile discrimination task where participants attended to stimuli delivered to one of two stimulated digits in the same hand, we investigated attention-based modulation of tactile ERP components and compared this between young and older adults. As previously mentioned, many ERP components can be modulated by attention and this has been shown even with early components representing somatosensory cortical processing (Bolton and Staines, 2011, Eimer and Forster, 2003, Schubert et al., 2008). Moreover, imaging work has shown a strong link between prefrontal activity and activity at these somatosensory processing stages (Staines, Graham, Black, & McIlroy, 2002) suggesting a prefrontal or top-down gating system based upon attention to task-relevant stimuli. Thus it seems very plausible that such prefrontal driven modulation of tactile ERP components could be susceptible to age-related deficits. We hypothesised that older adults would show diminished attention-based modulation of ERPs during a tactile discrimination task. Such disrupted modulation would be indicated by a loss in the difference between attended and unattended ERP components. Moreover, we postulated that this would most likely occur via reduced suppression of irrelevant stimuli and this effect would be evident early in the somatosensory processing stream. This would suggest reduced or absent attention-based modulation of early somatosensory processing within the cerebral cortex as a function of age. Finally, previous research investigating attention to somatosensory target stimuli revealed both slower and diminished P300 responses in older adults for attended targets possibly reflecting a relative weakening of cognitive processing (Yamaguchi & Knight, 1991). Therefore in accord with previous findings, we hypothesised that the P300 elicited in response to targets on the attended digit would be reduced in amplitude and reveal longer latencies in older subjects.

Section snippets

Participants

Twenty-five neurologically normal volunteers participated in the study after providing written informed consent. Participants were included in one of two experimental groups based upon age. Testing groups were as follows: (a) Young adults, YA (age range 20–39 years) and (b) Older adults OA (age range 62–89 years). Data from two participants were excluded due to excessive artefacts or an absence of specific ERP components. The final sample size for each group was as follows: YA (n = 12) and OA (n = 

Amplitudes

Grand average waveforms displaying the comparison of attention-based modulation between OA and YA groups are shown in Fig. 2 for 12 electrodes and more focally at C4 and CP4 in Fig. 3 (including scalp topography at the P100 peak). This data is depicted as bar graphs for each component in Fig. 4 for the P50, N70 and P100 and in Fig. 5 for the N140 and LLP. Two-way, mixed-model ANOVAs resulted in no significant main effects with age group (C4: F1,19 = 0.004, p = 0.949; CP4: F1,18 = 0.002, p = 0.968) or

Discussion

Neurologically intact, older adults showed diminished attention-based modulation of somatosensory ERPs during a tactile discrimination task when compared with younger adults. Several ERP components were modulated based upon attention in both age groups however the degree of this modulation differed. Most strikingly, non-attended stimuli resulted in greater P100 amplitudes for older adults compared with younger adults. Present data revealed a loss of attention-based modulation of somatosensory

Acknowledgements

This work was supported by research grants to WRS from the Natural Sciences and Engineering Research Council of Canada, the Canada Foundation for Innovation, and the Ontario Research Fund. DAEB was supported by postdoctoral fellowships from the Ontario Ministry of Research and Innovation and the Heart and Stroke Foundation Centre for Stroke Recovery. The authors thank Wendell Prime and Jeff Rice for constructing the vibrotactile stimulation device used in this study and Heather Lillico and Kate

References (51)

  • M. Eimer et al.

    The spatial distribution of attentional selectivity in touch: Evidence from somatosensory ERP components

    Clinical Neurophysiology

    (2003)
  • H. Hamalainen et al.

    Human somatosensory evoked potentials to mechanical pulses and vibration: Contributions of SI and SII somatosensory cortices to P50 and P100 components

    Electroencephalography and Clinical Neurophysiology

    (1990)
  • L. Hasher et al.

    Working memory, comprehension and aging: A review and a new view

  • Y. Iguchi et al.

    Attention induces reciprocal activity in the human somatosensory cortex enhancing relevant- and suppressing irrelevant inputs from fingers

    Clinical Neurophysiology

    (2005)
  • T.L. Jernigan et al.

    Effects of age on tissues and regions of the cerebrum and cerebellum

    Neurobiology of Aging

    (2001)
  • R.T. Knight et al.

    Prefrontal cortex regulates inhibition and excitation in distributed neural networks

    Acta Psychologica

    (1999)
  • F. Mauguiere et al.

    Activation of a distributed somatosensory cortical network in the human brain. A dipole modelling study of magnetic fields evoked by median nerve stimulation. Part I: Location and activation timing of SEF sources

    Electroencephalography and Clinical Neurophysiology

    (1997)
  • J. Polich

    Updating P300: An integrative theory of P3a and P3b

    Clinical Neurophysiology

    (2007)
  • W.R. Staines et al.

    Task-relevant modulation of contralateral and ipsilateral primary somatosensory cortex and the role of a prefrontal-cortical sensory gating system

    NeuroImage

    (2002)
  • M.C. Stoeckel et al.

    A fronto-parietal circuit for tactile object discrimination: An event-related fMRI study

    NeuroImage

    (2003)
  • K.B. Walhovd et al.

    The relationship between P3 and neuropsychological function in an adult life span sample

    Biological Psychology

    (2003)
  • S. Yamaguchi et al.

    Gating of somatosensory input by human prefrontal cortex

    Brain Research

    (1990)
  • S. Yamaguchi et al.

    Age effects on the P300 to novel somatosensory stimuli

    Electroencephalography and Clinical Neurophysiology

    (1991)
  • C.D. Yingling et al.

    Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami

    Electroencephalography and Clinical Neurophysiology

    (1976)
  • T. Allison et al.

    Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings

    Brain

    (1991)
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