Rhythmic Spontaneous Activity Mediates the Age-Related Decline in Somatosensory Function

Abstract

Sensory gating is a neurophysiological process whereby the response to a second stimulus in a pair of identical stimuli is attenuated, and it is thought to reflect the capacity of the CNS to preserve neural resources for behaviorally relevant stimuli. Such gating is observed across multiple sensory modalities and is modulated by age, but the mechanisms involved are not understood. In this study, we examined somatosensory gating in 68 healthy adults using magnetoencephalography (MEG) and advanced oscillatory and time-domain analysis methods. MEG data underwent source reconstruction and peak voxel time series data were extracted to evaluate the dynamics of somatosensory gating, and the impact of spontaneous neural activity immediately preceding the stimulation. We found that gating declined with increasing age and that older adults had significantly reduced gating relative to younger adults, suggesting impaired local inhibitory function. Most importantly, older adults had significantly elevated spontaneous activity preceding the stimulation, and this effect fully mediated the impact of aging on sensory gating. In conclusion, gating in the somatosensory system declines with advancing age and this effect is directly tied to increased spontaneous neural activity in the primary somatosensory cortices, which is likely secondary to age-related declines in local GABA inhibitory function.

Haptic exploration attenuates and alters somatosensory cortical oscillations

“…; Spooner et al . ). However, whether these frequency‐specific somatosensory cortical oscillations are modulated by haptic exploration remains unknown.…”

“…Furthermore, it has recently been shown that these neural oscillations are modulated across a broad frequency range (e.g. 10-75 Hz) following a pair of identical and successive peripheral somatosensations Wiesman et al 2017;Spooner et al 2018). However, whether these frequency-specific somatosensory cortical oscillations are modulated by haptic exploration remains unknown.…”

Methodological considerations for a better somatosensory gating paradigm: The impact of the inter-stimulus interval

“…This weakened response to stimuli presented in rapid succession is thought to reflect the brain’s capacity to filter irrelevant information to preserve neural resources for more behaviorally relevant stimuli ( Adler et al, 1982 , 1998 ; Cromwell et al, 2008 ; Nagamoto et al, 1989 , 1991 ; Venables, 1964 ). SG has been examined in many clinical populations and across multiple sensory modalities (e.g., auditory and somatosensory) and broadly is known to be aberrant in aging, as well as many psychiatric and neurological conditions (e.g., schizophrenia, bipolar disorder, cerebral palsy, neuroHIV ( Brinkman and Stauder, 2007 ; Cheng et al, 2015a ; Cheng et al, 2016a ; Cheng et al, 2015b ; Cheng and Lin, 2013 ; Kisley et al, 2003 ; Kurz et al, 2017 ; Light and Braff, 1999 ; Spooner et al, 2018 ; Spooner et al, 2019 ; Thoma et al, 2017 )). Historically, SG paradigms have used a paired-stimulus presentation design, whereby pairs of auditory tones or electrical stimulations are administered in close temporal proximity to evaluate gating in the auditory or somatosensory domain, respectively.…”

“…The ratio approach is the most common as it is less affected by individual differences in response amplitude across both stimulations. Importantly, regardless of the tested modality or clinical population, aberrations in SG are thought to reflect alterations in functional inhibitory processing ( Cheng et al, 2016b ; Cromwell et al, 2008 ; Gao et al, 2013 ; Spooner et al, 2018 , 2019 ), making the application of such protocols in human neurophysiology extremely desirable.…”

“…While the overall paired-pulse design of SG experiments has been in place for decades, there are a host of other experimental parameters that must be considered during task design, such as stimulus intensity, time between the individual stimuli, and time between the pairs. For example, it is exceedingly common for SG protocols to present the identical stimuli in rapid succession separated by a fixed, relatively short inter-stimulus interval (e.g., 500 ms), while the pairs of identical stimuli are separated by larger temporal windows (e.g., 5000 ms) that can be randomly jittered to eliminate anticipatory responses ( Cheng et al, 2016b ; Kurz et al, 2017 ; Spooner et al, 2019 ; Wiesman et al, 2017 ). These pairs of stimuli are always presented at identical intensities within the same person, to ease the interpretation of any experimental effects, and these intensities are often determined by individual-specific thresholds.…”