Elsevier

Clinical Neurophysiology

Volume 127, Issue 1, January 2016, Pages 655-663
Clinical Neurophysiology

Cortical correlates of response time slowing in older adults: ERP and ERD/ERS analyses during passive ankle movement

https://doi.org/10.1016/j.clinph.2015.05.003Get rights and content

Highlights

  • During passive ankle movement, older adults showed lower amplitude and longer latency of the N1 component than young adults, which correlated with their delayed response time.

  • Larger beta event-related desynchronization (ERD) in a response time task in older adults may be an indication of a higher cognitive effort to process weaker proprioceptive inputs (lower N1).

  • Attenuated beta event-related synchronization (ERS) in older adults may be related to changes in intracortical inhibitory activity.

Abstract

Objectives

The response time (RT) to kinesthetic perception has been used as a proprioceptive measurement, for example, in older individuals. However, the RT cannot provide information on impairments at specific stages of the respective sensorimotor processing. In the present study, electroencephalographic (EEG) signals were recorded during passive ankle movement with and without an associated perceptual task of movement detection. The main purpose was to analyze differences between young and older adults both in terms of RT and cortical responses. Putative differences in the latter were expected to point to changes in the processing associated with neural pathways or cortical regions in the older subjects.

Methods

The EEG activity of nineteen older (OA, 65–76 years) and 19 young adults (YA, 21–32 years) was recorded during passive ankle movement, without motor voluntary response (NVR, sensory condition), and during a condition with voluntary motor response (VR, with measurement of the RT). Event-related potentials (ERP) and beta event-related desynchronization/synchronization (ERD/ERS) were recorded and analyzed in both experimental conditions.

Results

The RT in OA was larger than in YA (P < 0.0001). EEG analyses showed that the N1 amplitude was larger in the VR than in the NVR condition (P = 0.006), whereas no difference for latency was obtained between conditions (P = 0.376). Comparisons between the groups revealed attenuated (P = 0.019) and delayed (P = 0.001) N1 in the OA group, irrespective of the condition (no interaction group vs condition). Only OA showed correlations between RT and N1, with significant correlation for both amplitude (r = −0.603, P = 0.006) and latency (r = 0.703, P = 0.001). The ERD/ERS analyses revealed a task-dependent group effect: in NVR, significant differences were obtained only for the ERS amplitude, which was attenuated in OA (P = 0.003). In VR, larger (P = 0.004) and delayed (P = 0.003) ERD and attenuated (P = 0.029) and delayed (P = 0.017) ERS peaks were observed in the older group.

Conclusions

The results suggest that a larger response time to proprioceptive stimuli in older adults is associated with a weaker and delayed proprioceptive afferent inflow to the cortex. In this scenario, older adults would need a higher cognitive effort (larger ERD) to process the sensory inputs when attempting to properly perform a sensorimotor task.

Significance

ERP and ERD/ERS measurements during kinesthetic assessment provide new insights on identification of the origin of sensorimotor slowing in older adults.

Introduction

Several studies have provided evidence that proprioceptive sense is reduced as a consequence of aging (for a review, see (Goble et al., 2009)) and that this change is associated with decreased performance in sensorimotor tasks such as posture and gait. For instance, reduced postural stability in older adults has been related to proprioceptive impairment in the lower limbs (Fitzpatrick and McCloskey, 1994, Lord and Ward, 1994, McChesney and Woollacott, 2000, Toledo and Barela, 2014).

The most common methods for examining the proprioceptive sense involve behavioral measurements such as replication of a predetermined target joint position either with the same (ipsilateral) or with the contralateral limb (Skinner et al., 1984, Lephart et al., 1997, Deshpande et al., 2003, Pickard et al., 2003, Amin and Herrington, 2014) and response time to motion sense (Thelen et al., 1998, Tomberg, 1999, Deshpande et al., 2003, Salles et al., 2011, Toledo and Barela, 2014). As measurements of performance, both are limited in quantifying possible proprioceptive impairment per se (e.g., proprioceptive loss due to aging or neuropathy) since both measurements can be also influenced by cognitive and motor factors. A promising approach for investigating the neurophysiological aspects of proprioceptive function is the association of passive joint movement to different techniques such as microneurography (Burke et al., 1988, Ribot-Ciscar et al., 2013), electroencephalography (EEG) (Cassim et al., 2001, Lewis and Byblow, 2002, Seiss et al., 2002, Keinrath et al., 2006), and transcranial magnetic stimulation (TMS) (Lewis et al., 2001, Lewis and Byblow, 2002). The combination of these techniques can be very useful in the study of how different stages of information transmission and processing are involved in a cognitive sensorimotor task. However, electrophysiological analyses during proprioceptive tasks are still little explored in older adults and, therefore, the specific impairments that lead to their lower performance in proprioceptive assessment (e.g., increased response time) remains to be determined.

Age-related impairments at specific stages of neural signal processing and generation during sensorimotor tasks were previously reported for other stimulus modalities (Yordanova et al., 2004). Analyses based on event-related potentials (ERPs) showed that increased response time to visual and auditory stimuli in older adults was correlated with late cortical processing related to response generation (i.e., motor-related potential) (Yordanova et al., 2004), but was not related to early sensory processing stages. Whether the origin of response time slowing in older adults is independent of stimulus modality is still unknown, thus, the results obtained for visual and auditory stimuli cannot be extrapolated to somatosensory stimuli.

Beyond ERP analyses, recent studies provided important clues concerning the stimulus processing during kinesthetic assessment by showing that specific cortical rhythms (e.g., beta band from 14 to 37 Hz) can be altered during passive joint movement (Cassim et al., 2001, Muller-Putz et al., 2007, Salles et al., 2011). Increased cortical activity at a specific frequency band is called event-related synchronization (ERS) (Pfurtscheller et al., 2006). Based on the evidence of reduced motor-evoked potential (MEP, assessed by TMS) at the same time of ERS occurrence during active movement, the cortical synchronization is interpreted as a cortical state of reduced excitability (Chen et al., 1998). The functional meaning of ERS during passive movements is not known precisely, but there is evidence that it also involves somatosensory processing, given that the ERS induced by passive index finger movement disappears after deafferentation by ischaemic nerve block (Cassim et al., 2001). On the other hand, reduced cortical activity at specific frequency bands is called event-related desynchronization (ERD) (Niedermeyer and Lopes da Silva, 1999) and has been associated with increased cortical excitability. ERD/ERS analyses can provide complementary data to the ERP findings and may clarify important aspects regarding the aging effects on the dynamics of brain oscillations during a sensorimotor task, such as passive ankle movement.

The goal of the present study was to investigate the cortical changes during the assessment of the proprioceptive system during passive ankle movement in young and older adults. For this purpose, ERP and ERD/ERS analyses were compared between conditions in which the subject was instructed either only to attend or to attend and respond (press a button) to the perception of passive ankle movement. The first condition provides specific information related to the sensory processes involved in the sensorimotor response time task. Additionally, the responses were compared between young and older adults in an effort to shed some light on the effects of aging on cortical processing of proprioceptive inputs associated with the ankle.

Section snippets

Participants

Nineteen older (OA, 70.3 ± 4.1 years; 65–76) and 19 young (YA, 28.5 ± 2.9 years; 21–32) right-footed adults (10 females in each group) participated in this study. They were recruited from graduate programs, local communities, and a cultural center for retirees. The older participants were chosen among those who had not been enrolled in any regular physical activity program (for at least three years), had not suffered any falls in the last two years, had no vestibular impairment, pain, visual,

Results

Mean values of the behavioral (RT) and electrophysiological N1 variables for both groups and both conditions are shown in Table 1. Behavioral results for the VR condition showed that RT was overall 47.48 ms larger in the older than in the young adults [F(1,36) = 27.037, P < 0.0001].

Discussion

Our results showed that brain electrophysiological measurements correlate with response time differences in the perception of passive ankle movement found between young and older adults. Comparisons between conditions VR and NVR provide important information for understanding the neural processing stages involved in ankle motion perception. These results are discussed below separately for N1 and ERD/ERS components.

Conclusions

From the combined results of ERP and ERD/ERS, we concluded that there are electrophysiological correlates at the cortical level of sensorimotor performance during assessment of ankle kinesthetic perception. The age-related delay in the response time to a predominantly proprioceptive stimulus generated by passive ankle motion is probably related to weaker and delayed proprioceptive afferent arrival at the cortex and also to slower cortical processes possibly associated with reduced selective

Acknowledgements

This research was funded by Grants from FAPESP (#2011/17193-0) and CNPq (#303313/2011-0).

DRT received a Ph.D. scholarship (Grant No. 2009/09286-9) and holds a Post-Doctoral Grant (Grant no. 2013/14667-7) from FAPESP.

Conflict of interest: The authors declare that there are no conflicts of interest.

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