Age-dependent modulation of the somatosensory network upon eye closure

Eye closure even in complete darkness can improve somatosensory perception by switching the brain to a uni-sensory processing mode. This causes an increased information flow between the thalamus and the somatosensory cortex while decreasing modulation by the visual cortex. Previous work suggests that these modulations are age-dependent and that the benefit in somatosensory performance due to eye closing diminishes with age. The cause of this age-dependency and to what extent somatosensory processing is involved remains unclear. Therefore, we intended to characterize the underlying age-dependent modifications in the interaction and connectivity of different sensory networks caused by eye closure. We performed functional MR-imaging with tactile stimulation of the right hand under the conditions of opened and closed eyes in healthy young and elderly participants. Conditional Granger causality analysis was performed to assess the somatosensory and visual networks, including the thalamus. Independent of age, eye closure improved the information transfer from the thalamus to and within the somatosensory cortex. However, beyond that, we found an age-dependent recruitment strategy. Whereas young participants were characterized by an optimized information flow within the relays of the somatosensory network, elderly participants revealed a stronger modulatory influence of the visual network upon the somatosensory cortex. Our results demonstrate that the modulation of the somatosensory and visual networks by eye closure diminishes with age and that the dominance of the visual system is more pronounced in the aging brain.

[1]  Stefan Brodoehl,et al.  Eye closure enhances dark night perceptions , 2015, Scientific Reports.

[2]  K. Amunts,et al.  Activation shift in elderly subjects across functional systems: an fMRI study , 2013, Brain Structure and Function.

[3]  Leslie G. Ungerleider,et al.  Age-related changes in cortical blood flow activation during visual processing of faces and location , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[5]  Dean Cvetkovic,et al.  The dark side of the alpha rhythm: fMRI evidence for induced alpha modulation during complete darkness , 2013, The European journal of neuroscience.

[6]  P. D. Spear,et al.  Neural bases of visual deficits during aging , 1993, Vision Research.

[7]  Tzu-Chen Yeh,et al.  Differential effects of stimulus intensity on peripheral and neuromagnetic cortical responses to median nerve stimulation , 2003, NeuroImage.

[8]  Claudio Babiloni,et al.  Comparison between SI and SII responses as a function of stimulus intensity , 2002, Neuroreport.

[9]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  H. C. Dijkerman,et al.  Somatosensory processes subserving perception and action , 2007, Behavioral and Brain Sciences.

[11]  O. Witte,et al.  Excitatory and inhibitory mechanisms underlying somatosensory habituation , 2014, Human brain mapping.

[12]  Jennifer L. Mozolic,et al.  Multisensory Integration and Aging , 2012 .

[13]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[14]  R. Cabeza,et al.  Que PASA? The posterior-anterior shift in aging. , 2008, Cerebral cortex.

[15]  O. Witte,et al.  The impact of eye closure on somatosensory perception in the elderly , 2015, Behavioural Brain Research.

[16]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[17]  S. Hayasaka,et al.  Aging and the interaction of sensory cortical function and structure , 2009, Human brain mapping.

[18]  M. Wallace,et al.  Enhanced multisensory integration in older adults , 2006, Neurobiology of Aging.

[19]  Anthony Randal McIntosh,et al.  Visual dominance and multisensory integration changes with age , 2013, NeuroImage.

[20]  R. Kahn,et al.  Human brain changes across the life span: A review of 56 longitudinal magnetic resonance imaging studies , 2012, Human brain mapping.

[21]  Martin Wiesmann,et al.  Eyes open and eyes closed as rest conditions: impact on brain activation patterns , 2004, NeuroImage.

[22]  W. Backes,et al.  Somatosensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention , 2000, Clinical Neurophysiology.

[23]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[24]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[25]  D. Yan,et al.  Ageing and hearing loss , 2007, The Journal of pathology.

[26]  Claudio Babiloni,et al.  Human secondary somatosensory cortex is involved in the processing of somatosensory rare stimuli: An fMRI study , 2008, NeuroImage.

[27]  C. G. Phillips,et al.  Projection from low‐threshold muscle afferents of hand and forearm to area 3a of baboon's cortex , 1971, The Journal of physiology.