Elsevier

Neurobiology of Aging

Volume 33, Issue 6, June 2012, Pages 1073-1084
Neurobiology of Aging

Regular paper
Aging of human supraspinal locomotor and postural control in fMRI

https://doi.org/10.1016/j.neurobiolaging.2010.09.022Get rights and content

Abstract

Standing, walking, and running are sensorimotor tasks that develop during childhood. Thereafter they function automatically as a result of a supraspinal network that controls spinal pattern generators. The present study used functional magnetic resonance imaging (fMRI) to investigate age-dependent changes in the supraspinal locomotor and postural network of normal subjects during mental imagery of locomotion and stance. Sixty healthy subjects (ages: 24–78 years), who had undergone a complete neurological, neuro-ophthalmological, and sensory examination to rule out disorders of balance and gait, were trained for the conditions lying, standing, walking, and running in order to imagine these conditions on command in 20-second sequences with the eyes closed while lying supine in an magnetic resonance imaging (MRI) scanner. The following blood oxygen level-dependent (BOLD) signal changes during locomotion and stance were found to be independent of age: (1) prominent activations in the supplementary motor areas, the caudate nuclei, visual cortical areas, vermal, and paravermal cerebellum; (2) significant deactivations in the multisensory vestibular cortical areas (posterior insula, parietoinsular vestibular gyrus, superior temporal gyrus), and the anterior cingulate during locomotion. The following differences in brain activation during locomotion and stance were age-dependent: relative increases in the cortical BOLD signals in the multisensory vestibular cortices, motion-sensitive visual cortices (MT/V5), and somatosensory cortices (right postcentral gyrus). In advanced age this multisensory activation was most prominent during standing, less during walking, and least during running. In conclusion, the functional activation of the basic locomotor and postural network, which includes the prefrontal cortex, basal ganglia, brainstem, and cerebellar locomotor centers, is preserved in the elderly. Two major age-dependent aspects of brain activation during locomotion and stance were found: the mechanism of cortical inhibitory reciprocal interaction between sensory systems during locomotion and stance declines in advanced age; and consequently, multisensory cortical control of locomotion and stance increases with age. These findings may indicate a more conscious locomotor and postural strategy in the elderly.

Introduction

Balance and gait disturbances have a considerable impact on the activities of daily life of the elderly. Falls are a major source of injury and morbidity: 20%–30% of older persons who fall suffer moderate to severe injuries that limit mobility and reduce the quality of life (Alexander et al., 1992). Older adults show increased postural sway in steady stance and have difficulty controlling displacement of the center of mass and center of pressure relative to their limits of stability (Maki and McIlroy, 1996, Tang and Woollacott, 1998). The mean and maximum velocity of gait decreases over age. This finding may be associated with frontal gray matter atrophy and the decline of striatal dopamine transport (Cham et al., 2008, Rosano et al., 2006, Rosano et al., 2008).

The network of locomotion and stance in the central nervous system is organized hierarchically, i.e., spinal pattern generators are controlled by supraspinal locomotor centers. This basic structure was preserved during the transition from quadrupedal to bipedal locomotion and stance (Dietz, 2002, Jahn et al., 2008a). However, human locomotion and stance are assumed to be under more supraspinal control than that in animals. Recently the supraspinal locomotor and postural network in young healthy subjects was identified using mental imagery of locomotion and stance in functional magnetic resonance imaging (fMRI). Cortical commands for locomotion originate in the supplementary motor cortices and are conveyed by the basal ganglia (mainly the caudate nucleus) to brainstem locomotor centers located in the pontomesencephalic tegmentum (Bakker et al., 2008, Jahn et al., 2004, Jahn et al., 2008b). The anatomical correlates in humans are probably the subthalamic nucleus and the pedunculopontine/cuneiform nucleus complex (Jenkinson et al., 2009). An intraindividual fMRI-positron emission tomography (PET) comparison confirmed that imagined and real locomotion paradigms are both capable of depicting the supraspinal locomotor network (La Fougère et al., 2010).

The control of locomotion and posture involves a complex interplay between the sensory and motor systems (Rossignol et al., 2006). Afferent sensory feedback plays a crucial role in adapting and modulating the operation of the locomotor network in the real environment. The cortical somatosensory input adapts locomotor activity for accurate foot placement during each step cycle (Armstrong, 1986, Christensen et al., 2000). Vestibular stimulation induces a phase-dependent modulation of the leg motor control during locomotion (Bent et al., 2004). The motor cortex conveys important visual commands during locomotion, which are needed for the proper adjustments of the gait to the features of the environment (Drew et al., 1996). Furthermore, an appropriate internal representation of the body in space during locomotion depends on the integration of vestibular, visual, and somatosensory information (Hlavacka et al., 1995, Maurer et al., 2000). During 2-foot ground support, somatosensory information can give a more reliable indication of body position than during the swing phase when 1 limb is in the air. The integration of vestibular information and somatosensory input during 2-foot support determines whether the movement of the body relative to the base of support results in the desired end position during walking.

During aging, these sensorimotor abilities may not only be affected by the decline of the peripheral nervous or neuromuscular systems, but especially by age-related changes of brain structure and function as well. Functional alterations of the cerebral processing of simple sensorimotor tasks during aging have been investigated by functional imaging (Heuninckx et al., 2008, Riecker et al., 2006, Ward et al., 2008). During motor tasks older adults exhibit additional activations in higher level sensorimotor cortical areas (Heuninckx et al., 2005). This suggests they increasingly rely for movement control on cognitive input and cortical sensory information processing. The engagement of additional sensory areas most likely reflects a compensatory mechanism for age-related sensorimotor decline (Heuninckx et al., 2008, Venkatraman et al., 2010). Whereas unimodal sensory ability declines with increasing age and older adults have decreased sensory cortical activity responses, the cortical representation of multisensory information seems to be enhanced during aging (Levine et al., 2000). In contrast, visual stimuli in young adults increase activity in the visual cortices while suppressing activity in other sensory modalities, e.g., auditory, somatosensory, and vestibular modalities (Alsius et al., 2005, Brandt et al., 1998, Laurienti et al., 2002). The underlying mechanism involved has been termed inhibitory reciprocal interaction. In older adults this inhibitory reciprocal interaction is reduced, while the sensory cortical areas are simultaneously activated during spatially and temporally coincident multisensory stimuli (Peiffer et al., 2009). The greatest multisensory-mediated benefits are generally seen when the individual stimuli are weak and close to the sensory threshold (Laurienti et al., 2006). Studies have also shown that as the effectiveness of unimodal stimuli decreases, the multisensory gain increases (Hairston et al., 2003).

An increased multisensory cortical integration may also serve to substitute for locomotor function transcortically. However, the age-related changes of cerebral sensorimotor processing during locomotion and stance have so far not been investigated. The present study aims to depict the supraspinal locomotor and postural network by having a group of healthy subjects of different ages mentally imagine locomotion and stance during fMRI. This may contribute to our understanding of the neurobiological correlates of stance and gait in the elderly and identify the mechanisms of dedifferentiation or compensation during these complex sensorimotor processes during aging.

Section snippets

Subjects

Sixty healthy adults (30 men, ages 24 to 78 years, mean age: 50.3 ± 23.8 years) without gait disorders were included in the study. All patients underwent a complete neurological and neuro-ophthalmological examination. Posturography was performed using a Kistler-platform as described earlier (Krafczyk et al., 2006). All subjects had normal test results. Vertigo and balance disorders in the past medical history were excluded by a structured questionnaire. All subjects gave their informed, written

Results

In the following, data are presented in 3 paragraphs: (1) the supraspinal locomotor and stance network in the elderly, (2) the age-related differences in this network, and (3) the mechanisms of age-dependent sensorimotor regulation during locomotion and stance.

Discussion

The present study revealed age-related changes of the brain network of locomotion and stance by means of mental imagery during fMRI. The major findings were the following. (1) the functional activation of the supraspinal locomotor network, which consists of the premotor cortex, basal ganglia, midline cerebellum, and pontomesencephalic tegmentum, is preserved during aging. (2) In advanced age multisensory cortical activation (vestibular, visual, somatosensory) increases; it is less prominent

Disclosure statement

The authors state that there are no actual or potential conflicts of interest.

The protocol of the study was approved by the Ethics Committee of the Ludwig-Maximilians-University of Munich. All subjects gave their informed, written consent to participate in the study.

Acknowledgements

The study was supported by the German Research Foundation (JA 1087/1-1), the German Federal Ministry of Education and Research (initiative IFBLMU) and the Hertie Foundation (Hertie Senior Professorship Neurosciences awarded to Professor Thomas Brandt). We thank Judy Benson for copyediting the manuscript.

References (49)

  • K. Jahn et al.

    Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging

    Neuroimage

    (2004)
  • S. Krafczyk et al.

    Artificial neural network: A new diagnostic posturographic tool for disorders of stance

    Clin. Neurophysiol

    (2006)
  • C. La Fougère et al.

    Real versus imagined locomotion: a [18F]-FDG-PET - fMRI comparison

    Neuroimage

    (2010)
  • P.J. Laurienti et al.

    Enhanced multisensory integration in older adults

    Neurobiol. Aging

    (2006)
  • B.K. Levine et al.

    Age-related differences in visual perceptiona PET study

    Neurobiol. Aging

    (2000)
  • B.E. Maki et al.

    Postural control in the older adult

    Clin. Geriatr. Med

    (1996)
  • C. Maurer et al.

    Vestibular, visual, and somatosensory contributions to human control of upright stance

    Neurosci. Lett

    (2000)
  • A. Riecker et al.

    Functional significance of age-related differences in motor activation patterns

    Neuroimage

    (2006)
  • V.K. Venkatraman et al.

    Executive control function, brain activation and white matter hyperintensities in older adults

    Neuroimage

    (2010)
  • N.S. Ward et al.

    Age-dependent changes in the neural correlates of force modulation: An fMRI study

    Neurobiol. Aging

    (2008)
  • B.H. Alexander et al.

    The cost and frequency of hospitalization for fall-related injuries in older adults

    Am. J. Public Health

    (1992)
  • D.M. Armstrong

    The supraspinal control of mammalian locomotion

    J. Physiol

    (1988)
  • D.M. Armstrong et al.

    Complex spikes in purkinje-cells of the paravermal part of the anterior lobe of the cat cerebellum during locomotion

    J. Physiol

    (1988)
  • L.R. Bent et al.

    When is vestibular information important during walking

    J. Neurophysiol

    (2004)
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