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Fnhum-12-00477 November 29, 2018 Time: 13:4 # 1 This is an electronic reprint of the original article. This reprint may differ from the original in pagination and typographic detail. Nurmi, Timo; Henriksson, Linda; Piitulainen, Harri Optimization of Proprioceptive Stimulation Frequency and Movement Range for fMRI Published in: FRONTIERS IN HUMAN NEUROSCIENCE DOI: 10.3389/fnhum.2018.00477 Published: 03/12/2018 Document Version Publisher's PDF, also known as Version of record Published under the following license: CC BY Please cite the original version: Nurmi, T., Henriksson, L., & Piitulainen, H. (2018). Optimization of Proprioceptive Stimulation Frequency and Movement Range for fMRI. FRONTIERS IN HUMAN NEUROSCIENCE, 12, 1-15. 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Powered by TCPDF (www.tcpdf.org) fnhum-12-00477 November 29, 2018 Time: 13:4 # 1 ORIGINAL RESEARCH published: 03 December 2018 doi: 10.3389/fnhum.2018.00477 Optimization of Proprioceptive Stimulation Frequency and Movement Range for fMRI Timo Nurmi1,2*, Linda Henriksson1,2 and Harri Piitulainen1,2 1 Department of Neuroscience and Biomedical Engineering (NBE), Aalto University, Espoo, Finland, 2 Aalto NeuroImaging, Aalto University, Espoo, Finland For vision, audition and tactile sense, the optimal stimulus frequency for fMRI is somewhat known. For proprioception, i.e., the “movement sense”, however, the optimal frequency is unknown. We studied the effect of passive-finger-movement frequency on proprioceptive fMRI responses using a novel pneumatic-movement actuator. Eleven healthy right-handed volunteers participated in the study. The movement actuator passively moved the participant’s right index finger at frequencies of 0.3, 1, 3, 6, 9, or 12 Hz in a blocked design. A functional localizer was used to define regions- of-interest in SI and SII cortices. In addition, effect of movement range on the fMRI responses was tested in a separate session with 1, 3, 5, and 7 mm movement ranges at a fixed 2 Hz frequency. In primary somatosensory (SI) cortex, the responses were stronger at 3 Hz than at 0.3 Hz (p < 0.001) or 1 Hz (p < 0.05), and at ≥6 Hz than 0.3 Hz (p < 0.001 for frequencies ≥ 6 Hz). In secondary somatosensory (SII) cortex, all movements, except at 0.3 Hz, elicited significant responses of similar strength. In addition, 6, 9, and 12-Hz movements elicited a significant offset response in both SI and SII cortices (p < 0.001–0.05). SI cortex required a total stimulation duration of 4 min Edited by: to elicit significant activations at the group-level whereas for SII cortex 1 min 20 s was Felix Blankenburg, Freie Universität Berlin, Germany sufficient. Increase in the movement range led to stronger responses in SI cortex, but Reviewed by: not in SII cortex. Movements above 3 Hz elicited the strongest SI cortex responses, and Matt J. N. Brown, increase in the movement range enhanced the response strength. We thus recommend California State University, Sacramento, United States that movements at 3–6 Hz with a movement range of 5 mm or higher to be used in future Ann Van de Winckel, studies of proprioception. Our results are in-line with previous fMRI and PET studies University of Minnesota Twin Cities, using tactile or median nerve stimulation at different stimulation frequencies. United States *Correspondence: Keywords: kinesthesia, passive movement, proprioception, somatosensory cortex, repetition rate, sensorimotor Timo Nurmi system, fMRI, movement range timo.nurmi@aalto.fi Received: 04 May 2018 INTRODUCTION Accepted: 14 November 2018 Published: 03 December 2018 The term proprioception, i.e., the position and movement sense of the body, was first introduced Citation: by Sherrington(1907), who described proprioceptors as: “In muscular receptivity we see the body Nurmi T, Henriksson L and itself acting as a stimulus to its own receptors—the proprioceptors” (for a review, see Proske and Piitulainen H (2018) Optimization of Gandevia, 2012). Proprioceptors are located in muscles and joints and are thus sensitive to changes Proprioceptive Stimulation Frequency and Movement Range for fMRI. Abbreviations: (f)MRI, (functional) magnetic resonance imaging; GTO, golgi tendon organ; ISI, inter-stimulus-interval; Front. Hum. Neurosci. 12:477. MEG, magnetoencephalography; PET, positron emission tomography; SI cortex, primary somatosensory cortex; SII cortex, doi: 10.3389/fnhum.2018.00477 secondary somatosensory cortex. Frontiers in Human Neuroscience| www.frontiersin.org 1 December 2018| Volume 12| Article 477 fnhum-12-00477 November 29, 2018 Time: 13:4 # 2 Nurmi et al. Optimization of Proprioceptive Stimulation in the internal state of the musculoskeletal system. For example, Proprioceptors have been stimulated in fMRI by using a MRI- muscle spindles are sensitive to changes in the length and stretch compatible pneumatic vibration on skin over a tendon. It has of the muscle, and GTOs are monitoring tension produced by been well established that ∼80 Hz vibration efficiently activates the muscle (Moore, 1984; for a review, see Proske and Gandevia, muscle spindles and produces a proprioceptive illusion of 2012). Proprioceptors include also joint receptors and even movement (Goodwin et al., 1972; Roll and Vedel, 1982). Similar some cutaneous receptors (Ferrell et al., 1987). Proprioception high-rate vibration activates SI cortex when measured using is crucial for continuous, smooth motor actions (Forget and fMRI (Montant et al., 2009; Goble et al., 2011). Proprioceptors Lamarre, 1987; Ghez et al., 1995; Messier et al., 2003). Thus, it can be stimulated at more “natural” rates by passively moving is not surprising that many motor disorders, such as cerebral the participant’s limbs. In fMRI studies, most often the passive palsy and Parkinson’s disease, are accompanied with deficits movements have been generated manually by the investigator in proprioception (Zia et al., 2000; for a review see Konczak (Carel et al., 2000; Guzzetta et al., 2007; Boscolo Galazzo et al., 2009). Despite its relevance to motor control and motor et al., 2014). The drawbacks of experimenter-evoked movements disorders, proprioceptive processing in the human brain is still are variable stimulus frequency and amplitude. A more stable inadequately understood. approach is to use movement actuators that passively move the Consequently, the optimal parameters for proprioceptive participant’s limb. Previous studies have used MRI-compatible stimulation to elicit the maximal hemodynamic fMRI responses device, capable to move index finger along one axis (Van de are unknown. Selecting frequency of sensory stimuli that Winckel et al., 2013a) or two axes (i.e., both vertically and maximizes the brain activation in fMRI and minimizes scanning horizontally). The two-dimensional passive movements allows time enables efficient experimental setup. In the visual domain, discrimination tasks of shapes such as rectangles and triangles, strongest responses are obtained by a flickering 8–15 Hz stimulus which have been investigated in healthy participants, patients in primary visual cortex for both PET (Fox and Raichle, 1984) with stroke, and children with cerebral palsy (Van de Winckel and fMRI (Kwong et al., 1992). et al., 2005, 2012, 2013b). However, until now, only fixed Optimal stimulation frequency might also depend on the movement frequency has been applied in fMRI-studies (Weiller brain region in question. For example, the optimal parameters et al., 1996; Yu et al., 2008, 2011; Van de Winckel et al., 2013a; differ between the visual areas (Singh et al., 2000; Henriksson Tang et al., 2015). In addition to functional studies, a robotic et al., 2008). The same phenomenon has been observed for device has also been used to asses proprioceptive capability auditory stimuli. Response in lower-level regions of the auditory which was then correlated to diffusion tensor imaging (DTI) cortex, such as the inferior colliculus, increase as with stimulation results in children with perinatal stroke and cerebral palsy (see frequency, whereas the higher-level regions, such as medial Kuczynski et al., 2017, 2018). Moreover, motor system decline geniculate body and superior temporal gyrus, initially increase and proprioception has been studied with resting state fMRI with stimulation frequency from 2 to 10 Hz (Heschl’s gyrus) (Mathys et al., 2014). In MEG which measures the neuronal or from 1 to 2 Hz (Superior temporal gyrus) but then begin activity more directly (Hämäläinen et al., 1993), the optimal to decrease with further increase in the stimulation frequency ISI in eliciting the strongest proprioceptive responses in a from 10 to 35 Hz (Heschl’s gyrus) or from 2 to 35 Hz (Superior given time appears to lay within 1.5–3.0 s for index-finger temporal gyrus; Harms and Melcher, 2002). movements (Smeds et al., 2017). However, clear MEG responses Optimal stimulation frequency for somatosensory senses has are detected even at 12-Hz movements (Piitulainen et al., been studied in fMRI using tactile stimulation and electric 2015). median nerve stimulation. When using tactile stimulation, the The primary aim of this study was to determine the optimal Brodmann
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