The Right Supramarginal Gyrus Is Important for Proprioception in Healthy and Stroke-Affected Participants: A Functional MRI Study

I have no clue if this area was damaged in my stroke. My doctors told me nothing of what my stroke damage entailed. My proprioception is pretty bad on my left side, so it could be this or the underlying white matter was damaged.
http://journal.frontiersin.org/article/10.3389/fneur.2015.00248/full?

Ettie Ben-Shabat^1,2*, Thomas A. Matyas^1,2, Gaby S. Pell¹, Amy Brodtmann^1† and Leeanne M. Carey^1,2†

• ¹Neurorehabilitation and Recovery, Stroke, Florey Institute of Neuroscience and Mental Health, Melbourne, VIC, Australia
• ²Occupational Therapy, School of Allied Health, College of Science, Health and Engineering, La Trobe University, Melbourne, VIC, Australia

Human proprioception is essential for motor control, yet its central processing is still debated. Previous studies of passive movements and illusory vibration have reported inconsistent activation patterns related to proprioception, particularly in high-order sensorimotor cortices. We investigated brain activation specific to proprioception, its laterality, and changes following stroke. Twelve healthy and three stroke-affected individuals with proprioceptive deficits participated. Proprioception was assessed clinically with the Wrist Position Sense Test, and participants underwent functional magnetic resonance imaging scanning. An event-related study design was used, where each proprioceptive stimulus of passive wrist movement was followed by a motor response of mirror ­copying with the other wrist. Left (LWP) and right (RWP) wrist proprioception were tested separately. Laterality indices (LIs) were calculated for the main cortical regions activated during proprioception. We found proprioception-related brain activation in high-order sensorimotor cortices in healthy participants especially in the supramarginal gyrus (SMG LWP z = 4.51, RWP z = 4.24) and the dorsal premotor cortex (PMd LWP z = 4.10, RWP z = 3.93). Right hemispheric dominance was observed in the SMG (LI LWP mean 0.41, SD 0.22; RWP 0.29, SD 0.20), and to a lesser degree in the PMd (LI LWP 0.34, SD 0.17; RWP 0.13, SD 0.25). In stroke-affected participants, the main difference in proprioception-related brain activation was reduced laterality in the right SMG. Our findings indicate that the SMG and PMd play a key role in proprioception probably due to their role in spatial processing and motor control, respectively. The findings from stroke-­affected individuals suggest that decreased right SMG function may be associated with decreased proprioception. We recommend that clinicians pay particular attention to the assessment and rehabilitation of proprioception following right hemispheric lesions.

Introduction

Limb proprioception refers to knowledge of the spatial location of one’s limb in the absence of vision. Proprioception is vital for motor control (1), particularly of the upper limbs (2). It is essential for the control of coordinated movements, especially small or precise movements, and for motor skill acquisition (3). Hence, proprioceptive deficits in the upper limbs are associated with decreased function (1). Despite the importance of proprioception for function, it remains unclear which brain regions beyond the primary sensorimotor cortices (SIMIs) are involved in the processing of proprioception and how this brain activation is altered following focal brain lesions associated with proprioceptive deficits.

Researchers studying brain activation during passive movements of the elbow (4, 5), wrist (6, 7), hand (8), and finger (9, 10) have identified activation in the contralateral primary somatosensory (SI) and motor (MI) cortices and the inferior parietal lobe (IPL). However, investigators disagreed on the pattern (contralateral, ipsilateral, or both) and exact location of activation [supramarginal gyrus (SMG) or the secondary somatosensory cortex (SII)]. In contrast, neurophysiological studies of primates, identified the superior parietal lobe as a key region for the processing of proprioception (11, 12). The ability of current brain imaging paradigms to investigate proprioceptive specific processing, and in particular the contribution from higher order brain regions, requires careful consideration and design.

Inconsistent proprioception-related brain activation has also been reported in high-order motor cortices including the supplementary motor area (SMA), cerebellum (6, 8), and the premotor cortex (PMC) (5, 6, 8). Variations in proprioception-related brain activation may have been due to the fact that brain imaging studies of passive movements varied in paradigm design. In some cases, the support of the moving limb was suboptimal and may have introduced significant tactile stimulation (6, 8, 10), thus generating confounding brain activation.

Proprioception-related brain activation has also been studied using illusory vibrations. This is vibration of a tendon at a frequency between 70 and 100Hz, which creates an illusion of movement (13). Early findings from illusory vibration studies emphasized activation in motor cortices including: MI, SMA, PMC, and the cingulate motor area (14, 15). Later, researchers also identified brain activation in the IPL (5, 16–18). However, as was the case with passive movements, reported activation varied in location, with reports of activation in the parietal operculum (5, 15, 17) or the SMG (16, 18). Hemispheric bias was also controversial with some researchers reporting bilateral activation (16, 18), while others report a right hemisphere dominance (15, 17).

Illusory vibrations provide different peripheral stimuli to passive movements. The stimulus is large phasic and of uniform frequency in the primary afferent fibers of the muscle spindles (19, 20). Minimal, if any, stimulation is produced in the secondary fibers of the muscle spindles and the joint receptors (19, 20). In contrast, passive movements produce multifrequency phasic and tonic stimulation of the primary afferent fibers in the muscle spindles (21). Secondary fibers of the muscle spindles and joint receptors are also stimulated (21–23). It is possible that different peripheral stimuli were associated with differential brain activation (5). In such circumstances, brain activation during passive movements is likely to reflect the central processing of proprioception more accurately than illusory vibration.

An important limitation of both passive movement and illusory vibration brain imaging studies of proprioception is that participants were not required to provide accurate and measurable responses to the proprioceptive stimuli during scanning. Responses to proprioceptive stimuli are important for two reasons. First, by asking participants for accurate responses to proprioceptive stimuli (and monitoring the responses), examiners ensure that participants adequately engage in proprioceptive information processing. Second, the response requirement introduces a certain degree of difficulty to the proprioceptive task, which would not have been present if responses were not required. Increased task difficulty is desirable due to the associated increase in cortical activation (24, 25).

In healthy participants, findings from behavioral studies have suggested asymmetry in the accuracy of proprioception from the right and left limbs (26–28). Asymmetry in behavioral measures suggests hemispheric dominance and thus asymmetry in proprioception-related brain activation. Brain activation studies of illusory vibration stimulation confirmed right hemispheric dominance (15, 17, 18). Brain activation in the IPL and inferior frontal gyrus was found in all three studies, but the exact loci of activation and degree of laterality (i.e., right hemispheric or bilateral activation) varied. None of the brain imaging studies of passive movements investigated laterality of proprioception.

Quantitative behavioral measures of proprioception in stroke-affected individuals have shown deficits in about 50% of the participants (1, 29). Considering the adverse effect of proprioceptive deficits on function (1), it is important not only to understand the central processing of proprioception in healthy participants but also how it changes following brain lesions associated with proprioceptive deficits. This is because proprioception can be rehabilitated (30–32) with associated changes in brain activation (33) and improvement in function (34).

The current study was designed to investigate the brain–behavior relationship of proprioception. The research questions were:

(1) Which high-order brain areas are important for early coding of natural proprioceptive stimuli?

(2) Is proprioception-related brain activation lateralized, and if so in which areas?

(3) How does proprioception-related brain activation in stroke-affected individuals with proprioceptive deficits differ from that of healthy participants?

To answer these questions, we designed an event-related functional magnetic resonance imaging (fMRI) study with a controlled proprioceptive stimulus and response paradigm. The study was exploratory with data-driven laterality analyses.

First, proprioceptive stimuli were delivered with maximal limb support and minimal tactile stimulation to eliminate confounding brain activation. Second, participants were required to respond accurately to each proprioceptive stimulus for optimal brain activation related to attended proprioceptive information processing. Third, the paradigm and analyses were designed to show brain activation at the beginning of a proprioception task during the coding of proprioceptive stimuli. We hypothesized that coding proprioception would involve high-order somatosensory cortices in the parietal lobe including the IPL, the SII, and the superior parietal lobe. We also hypothesized that proprioception-related brain activation would be found in high-order motor cortices in the frontal lobe including the PMC, SMA, and cingulate motor cortex. The second hypothesis was that proprioception-related brain activation would be lateralized to the right hemisphere, particularly the high-order cortices. Finally, we hypothesized that laterality would decrease following stroke which affected proprioception.

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