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  • 1.
    Dimitriou, M
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Edin, Benoni B
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Discharges in Human Muscle Receptor Afferents during Block Grasping2008In: Journal of Neuroscience, ISSN 0270-6474, E-ISSN 1529-2401, Vol. 28, no 48, p. 12632-12642Article in journal (Refereed)
  • 2.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Crosstalk proposal: there is much to gain from the independent control of human muscle spindles2021In: Journal of Physiology, ISSN 0022-3751, E-ISSN 1469-7793, Vol. 599, no 10, p. 2501-2504Article in journal (Refereed)
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  • 3.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Enhanced Muscle Afferent Signals during Motor Learning in Humans2016In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 26, no 8, p. 1062-1068Article in journal (Refereed)
    Abstract [en]

    Much has been revealed concerning human motor learning at the behavioral level [1, 2], but less is known about changes in the involved neural circuits and signals. By examining muscle spindle responses during a classic visuomotor adaptation task [3-6] performed by fully alert humans, I found substantial modulation of sensory afferent signals as a function of adaptation state. Specifically, spindle control was independent of concurrent muscle activity but was specific to movement direction (representing muscle lengthening versus shortening) and to different stages of learning. Increased spindle afferent responses to muscle stretch occurring early during learning reflected individual error size and were negatively related to subsequent antagonist activity (i.e., 60-80 ms thereafter). Relative increases in tonic afferent output early during learning were predictive of the subjects' adaptation rate. I also found that independent spindle control during sensory realignment (the "washout" stage) induced afferent signal "linearization" with respect to muscle length (i.e., signals were more tuned to hand position). The results demonstrate for the first time that motor learning also involves independent and state-related modulation of sensory mechanoreceptor signals. The current findings suggest that adaptive motor performance also relies on the independent control of sensors, not just of muscles. I propose that the "gamma" motor system innervating spindles acts to facilitate the acquisition and extraction of task-relevant information at the early stages of sensorimotor adaptation. This designates a more active and targeted role for the human proprioceptive system during motor learning.

  • 4.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Human Muscle Spindle Sensitivity Reflects the Balance of Activity between Antagonistic Muscles2014In: Journal of Neuroscience, ISSN 0270-6474, E-ISSN 1529-2401, Vol. 34, no 41, p. 13644-13655Article in journal (Refereed)
    Abstract [en]

    Muscle spindles are commonly considered as stretch receptors encoding movement, but the functional consequence of their efferent control has remained unclear. The "alpha-gamma coactivation" hypothesis states that activity in a muscle is positively related to the output of its spindle afferents. However, in addition to the above, possible reciprocal inhibition of spindle controllers entails a negative relationship between contractile activity in one muscle and spindle afferent output from its antagonist. By recording spindle afferent responses from alert humans using microneurography, I show that spindle output does reflect antagonistic muscle balance. Specifically, regardless of identical kinematic profiles across active finger movements, stretch of the loaded antagonist muscle (i.e., extensor) was accompanied by increased afferent firing rates from this muscle compared with the baseline case of no constant external load. In contrast, spindle firing rates from the stretching antagonist were lowest when the agonist muscle powering movement (i.e., flexor) acted against an additional resistive load. Stepwise regressions confirmed that instantaneous velocity, extensor, and flexor muscle activity had a significant effect on spindle afferent responses, with flexor activity having a negative effect. Therefore, the results indicate that, as consequence of their efferent control, spindle sensitivity (gain) to muscle stretch reflects the balance of activity between antagonistic muscles rather than only the activity of the spindle-bearing muscle.

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  • 5.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Human muscle spindles are wired to function as controllable signal-processing devices2022In: eLIFE, E-ISSN 2050-084X, Vol. 11, article id e78091Article in journal (Refereed)
    Abstract [en]

    Muscle spindles are encapsulated sensory organs found in most of our muscles. Prevalent models of sensorimotor control assume the role of spindles is to reliably encode limb posture and movement. Here, I argue that the traditional view of spindles is outdated. Spindle organs can be tuned by spinal γ motor neurons that receive top-down and peripheral input, including from cutaneous afferents. A new model is presented, viewing γ motor activity as an intermediate coordinate transformation that allows multimodal information to converge on spindles, creating flexible coordinate representations at the level of the peripheral nervous system. That is, I propose that spindles play a unique overarching role in the nervous system: that of a peripheral signal-processing device that flexibly facilitates sensorimotor performance, according to task characteristics. This role is compatible with previous findings and supported by recent studies with naturalistically active humans. Such studies have so far shown that spindle tuning enables the independent preparatory control of reflex muscle stiffness, the selective extraction of information during implicit motor adaptation, and for segmental stretch reflexes to operate in joint space. Incorporation of advanced signal-processing at the periphery may well prove a critical step in the evolution of sensorimotor control theories.

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  • 6.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Rebuttal from Michael Dimitriou2021In: Journal of Physiology, ISSN 0022-3751, E-ISSN 1469-7793, Vol. 599, no 10, p. 2509-2510Article in journal (Refereed)
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  • 7.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Task-Dependent Modulation of Spinal and Transcortical Stretch Reflexes Linked to Motor Learning Rate2018In: Behavioral Neuroscience, ISSN 0735-7044, E-ISSN 1939-0084, Vol. 132, no 3, p. 194-209Article in journal (Refereed)
    Abstract [en]

    It is generally believed that task-dependent control of body configuration ("posture") is achieved by adjusting voluntary motor activity and transcortical "long-latency" reflexes. Spinal monosynaptic circuits are thought not to be engaged in such task-level control. Similarly, being in a state of motor learning has been strongly associated only with an upregulation of feedback responses at transcortical latencies and beyond. In two separate experiments, the current study examined the task-dependent modulation of stretch reflexes by perturbing the hand of human subjects while they were waiting for a "Go" signal to move at the different stages of a classic kinematic learning task (visuomotor rotation). Although the subjects had to resist all haptic perturbations equally across task stages, the study leveraged that task-dependent feedback controllers may already be "loaded" at the movement anticipation stage. In addition to an upregulation of reflex gains during early exposure to the visual distortion, I found a relative inhibition of reflex responses in the "washout" stage (sensory realignment state). For more distal muscles (brachioradialis) this inhibition also extended to the monosynaptic reflex response ("R1"). Moreover, these R1 gains reflected individual motor learning performance in the visuomotor task. The results demonstrate that the system's "control policy" in visuomotor adaptation can also include inhibition of proprioceptive reflexes, and that aspects of this policy can affect monosynaptic spinal circuits. The latter finding suggests a novel form of state-related control, probably realized by independent control of fusimotor neurons, through which segmental circuits can tune to higher-level features of a sensorimotor task.

  • 8.
    Dimitriou, Michael
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Edin, Benoni B
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Human muscle spindles act as forward sensory models2010In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 20, no 19, p. 1763-1767Article in journal (Refereed)
    Abstract [en]

    Modern theories of motor control incorporate forward models that combine sensory information and motor commands to predict future sensory states. Such models circumvent unavoidable neural delays associated with on-line feedback control. Here we show that signals in human muscle spindle afferents during unconstrained wrist and finger movements predict future kinematic states of their parent muscle. Specifically, we show that the discharges of type Ia afferents are best correlated with the velocity of length changes in their parent muscles approximately 100-160 ms in the future and that their discharges vary depending on motor sequences in a way that cannot be explained by the state of their parent muscle alone. We therefore conclude that muscle spindles can act as "forward sensory models": they are affected both by the current state of their parent muscle and by efferent (fusimotor) control, and their discharges represent future kinematic states. If this conjecture is correct, then sensorimotor learning implies learning how to control not only the skeletal muscles but also the fusimotor system.

  • 9.
    Franklin, Sae
    et al.
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany.
    Leib, Raz
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Franklin, David W.
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany; Munich Institute of Robotics and Machine Intelligence (MIRMI), Technical University of Munich, Munich, Germany; Munich Data Science Institute (MDSI), Technical University of Munich, Munich, Germany.
    Congruent visual cues speed dynamic motor adaptation2023In: Journal of Neurophysiology, ISSN 0022-3077, E-ISSN 1522-1598, Vol. 130, no 2, p. 319-331Article in journal (Refereed)
    Abstract [en]

    Motor adaptation to novel dynamics occurs rapidly using sensed errors to update the current motor memory. This adaption is strongly driven by proprioceptive and visual signals that indicate errors in the motor memory. Here, we extend this previous work by investigating whether the presence of additional visual cues could increase the rate of motor adaptation, specifically when the visual motion cue is congruent with the dynamics. Six groups of participants performed reaching movements while grasping the handle of a robotic manipulandum. A visual cue (small red circle) was connected to the cursor (representing the hand position) via a thin red bar. After a baseline, a unidirectional (3 groups) or bidirectional (3 groups) velocity-dependent force field was applied during the reach. For each group, the movement of the red object relative to the cursor was either congruent with the force field dynamics, incongruent with the force field dynamics, or constant (fixed distance from the cursor). Participants adapted more to the unidirectional force fields than to the bidirectional force field groups. However, across both force fields, groups in which the visual cues matched the type of force field (congruent visual cue) exhibited higher final adaptation level at the end of learning than the control or incongruent conditions. In all groups, we observed that an additional congruent cue assisted the formation of the motor memory of the external dynamics. We then demonstrate that a state estimation-based model that integrates proprioceptive and visual information can successfully replicate the experimental data.NEW & NOTEWORTHY We demonstrate that adaptation to novel dynamics is stronger when additional online visual cues that are congruent with the dynamics are presented during adaptation, compared with either a constant or incongruent visual cue. This effect was found regardless of whether a bidirectional or unidirectional velocity-dependent force field was presented to the participants. We propose that this effect might arise through the inclusion of this additional visual cue information within the state estimation process.

  • 10.
    Papaioannou, Stylianos
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Goal-dependent tuning of muscle spindle receptors during movement preparation2021In: Science Advances, E-ISSN 2375-2548, Vol. 7, no 9, article id eabe0401Article in journal (Refereed)
    Abstract [en]

    Voluntary movements are believed to undergo preparation before they are executed. Preparatory activity can benefit reaction time and the quality of planned movements, but the neural mechanisms at work during preparation are unclear. For example, there are no overt changes in muscle force during preparation. Here, using an instructed-delay manual task, we demonstrate a decrease in human muscle afferent activity (primary spindles) when preparing to reach targets in directions associated with stretch of the spindle-bearing muscle. This goal-dependent modulation of proprioceptors began early after target onset but was markedly stronger at the latter parts of the preparatory period. Moreover, whole-arm perturbations during reach preparation revealed a modulation of stretch reflex gains (shoulder and upper arm muscles) that reflected the observed changes in spindle activity. We suggest that one function of central preparatory activity is to tune muscle stiffness according to task goals via the independent control of muscle spindle sensors.

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  • 11.
    Papaioannou, Stylianos
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Muscle spindle function in muscular dystrophy: A potential target for therapeutic intervention2020In: Journal of Physiology, ISSN 0022-3751, E-ISSN 1469-7793, Vol. 598, no 8, p. 1433-1434Article in journal (Other academic)
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  • 12.
    Torell, Frida
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Franklin, Sae
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany.
    Franklin, David W.
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany; Munich Institute of Robotics and Machine Intelligence (MIRMI), Technical University of Munich, Munich, Germany; Munich Data Science Institute (MDSI), Technical University of Munich, Munich, Germany.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Assistive loading promotes goal-directed tuning of stretch reflex gains2023In: eNeuro, E-ISSN 2373-2822, Vol. 10, no 2, article id ENEURO.0438-22.2023Article in journal (Refereed)
    Abstract [en]

    Voluntary movements are prepared before they are executed. Preparatory activity has been observed across the CNS and recently documented in first-order neurons of the human PNS (i.e., in muscle spindles). Changes seen in sensory organs suggest that independent modulation of stretch reflex gains may represent an impor-tant component of movement preparation. The aim of the current study was to further investigate the preparatory modulation of short-latency stretch reflex responses (SLRs) and long-latency stretch reflex responses (LLRs) of the dominant upper limb of human subjects. Specifically, we investigated how different target pa-rameters (target distance and direction) affect the preparatory tuning of stretch reflex gains in the context of goal-directed reaching, and whether any such tuning depends on preparation duration and the direction of background loads. We found that target distance produced only small variations in reflex gains. In contrast, both SLR and LLR gains were strongly modulated as a function of target direction, in a manner that facili-tated the upcoming voluntary movement. This goal-directed tuning of SLR and LLR gains was present or enhanced when the preparatory delay was sufficiently long (.250 ms) and the homonymous muscle was unloaded [i.e., when a background load was first applied in the direction of homonymous muscle action (as-sistive loading)]. The results extend further support for a relatively slow-evolving process in reach preparation that functions to modulate reflexive muscle stiffness, likely via the independent control of fusimotor neurons. Such control can augment voluntary goal-directed movement and is triggered or enhanced when the homonymous muscle is unloaded.

  • 13.
    Torell, Frida
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Franklin, Sae
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany.
    Franklin, David W.
    Neuromuscular Diagnostics, Department of Sport and Health Sciences, Technical University of Munich, Munich, Germany; Munich Institute of Robotics and Machine Intelligence (MIRMI), Technical University of Munich, Munich, Germany; Munich Data Science Institute (MDSI), Technical University of Munich, Munich, Germany.
    Dimitriou, Michael
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Goal-directed modulation of stretch reflex gains is reduced in the non-dominant upper limb2023In: European Journal of Neuroscience, ISSN 0953-816X, E-ISSN 1460-9568, Vol. 58, no 9, p. 3981-4001Article in journal (Refereed)
    Abstract [en]

    Most individuals experience their dominant arm as being more dexterous than the non-dominant arm, but the neural mechanisms underlying this asymmetry in motor behaviour are unclear. Using a delayed-reach task, we have recently demonstrated strong goal-directed tuning of stretch reflex gains in the dominant upper limb of human participants. Here, we used an equivalent experimental paradigm to address the neural mechanisms that underlie the preparation for reaching movements with the non-dominant upper limb. There were consistent effects of load, preparatory delay duration and target direction on the long latency stretch reflex. However, by comparing stretch reflex responses in the non-dominant arm with those previously documented in the dominant arm, we demonstrate that goal-directed tuning of short and long latency stretch reflexes is markedly weaker in the non-dominant limb. The results indicate that the motor performance asymmetries across the two upper limbs are partly due to the more sophisticated control of reflexive stiffness in the dominant limb, likely facilitated by the superior goal-directed control of muscle spindle receptors. Our findings therefore suggest that fusimotor control may play a role in determining performance of complex motor behaviours and support existing proposals that the dominant arm is better supplied than the non-dominant arm for executing more complex tasks, such as trajectory control.

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