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  • 1.
    Johansson, Anders Sixten
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Pruszynski, J Andrew
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Edin, Benoni Benjamin
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Westberg, Karl-Gunnar
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Biting intentions modulate digastric reflex responses to sudden unloading of the jaw2014In: Journal of Neurophysiology, ISSN 0022-3077, E-ISSN 1522-1598, Vol. 112, no 5, p. 1067-1073Article in journal (Refereed)
    Abstract [en]

    Reflex responses in jaw opening muscles can be evoked when a brittle object cracks between the teeth and suddenly unloads the jaw. We hypothesized that this reflex response is flexible and, as such, is modulated according to the instructed goal of biting through an object. Study participants performed two different biting tasks when holding a peanut-half stacked on a chocolate piece between their incisors. In one task, they were asked to split the peanut-half only (single-split task) and, in the other task, they were asked to split both the peanut and the chocolate in one action (double-split task). In both tasks, the peanut split evoked a jaw opening muscle response, quantified from EMG recordings of the digastric muscle in a window 20-60 ms following peanut split. Consistent with our hypothesis, we found that the jaw opening muscle response in the single-split trials was about twice the size of the jaw opening muscle response in the double-split trials. A linear model that predicted the jaw opening muscle response on a single trial basis indicated that task settings played a significant role in this modulation but also that the pre-split digastric muscle activity contributed to the modulation. These findings demonstrate that, like reflex responses to mechanical perturbations in limb muscles, reflex responses in jaw muscles not only show gain-scaling but also are modulated by subject intent.

  • 2. Maeda, Rodrigo S.
    et al.
    Cluff, Tyler
    Gribble, Paul L.
    Pruszynski, J. Andrew
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Brain and Mind Institute, Western University, London, Ontario, Canada; Robarts Research Institute, Western University, London, Ontario, Canada; Department of Psychology, Western University, London, Ontario, Canada; Department of Physiology and Pharmacology, Western University, London, Ontario, Canada.
    Compensating for intersegmental dynamics across the shoulder, elbow, and wrist joints during feedforward and feedback control2017In: Journal of Neurophysiology, ISSN 0022-3077, E-ISSN 1522-1598, Vol. 118, no 4, p. 1984-1997Article in journal (Refereed)
    Abstract [en]

    Moving the arm is complicated by mechanical interactions that arise between limb segments. Such intersegmental dynamics cause torques applied at one joint to produce movement at multiple joints, and in turn, the only way to create single joint movement is by applying torques at multiple joints. We investigated whether the nervous system accounts for intersegmental limb dynamics across the shoulder, elbow, and wrist joints during self-initiated planar reaching and when countering external mechanical perturbations. Our first experiment tested whether the timing and amplitude of shoulder muscle activity account for interaction torques produced during single-joint elbow movements from different elbow initial orientations and over a range of movement speeds. We found that shoulder muscle activity reliably preceded movement onset and elbow agonist activity, and was scaled to compensate for the magnitude of interaction torques arising because of forearm rotation. Our second experiment tested whether elbow muscles compensate for interaction torques introduced by single-joint wrist movements. We found that elbow muscle activity preceded movement onset and wrist agonist muscle activity, and thus the nervous system predicted interaction torques arising because of hand rotation. Our third and fourth experiments tested whether shoulder muscles compensate for interaction torques introduced by different hand orientations during self-initiated elbow movements and to counter mechanical perturbations that caused pure elbow motion. We found that the nervous system predicted the amplitude and direction of interaction torques, appropriately scaling the amplitude of shoulder muscle activity during self-initiated elbow movements and rapid feedback control. Taken together, our results demonstrate that the nervous system robustly accounts for intersegmental dynamics and that the process is similar across the proximal to distal musculature of the arm as well as between feedforward (i.e., self- initiated) and feedback (i.e., reflexive) control. NEW & NOTEWORTHY Intersegmental dynamics complicate the mapping between applied joint torques and the resulting joint motions. We provide evidence that the nervous system robustly predicts these intersegmental limb dynamics across the shoulder, elbow, and wrist joints during reaching and when countering external perturbations.

  • 3.
    Nordmark, Per F.
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Pruszynski, J. Andrew
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Johansson, Roland S.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    BOLD Responses to Tactile Stimuli in Visual and Auditory Cortex Depend on the Frequency Content of Stimulation2012In: Journal of cognitive neuroscience, ISSN 0898-929X, E-ISSN 1530-8898, Vol. 24, no 10, p. 2120-2134Article in journal (Refereed)
    Abstract [en]

    Although some brain areas preferentially process information from a particular sensory modality, these areas can also respond to other modalities. Here we used fMRI to show that such responsiveness to tactile stimuli depends on the temporal frequency of stimulation. Participants performed a tactile threshold-tracking task where the tip of either their left or right middle finger was stimulated at 3, 20, or 100 Hz. Whole-brain analysis revealed an effect of stimulus frequency in two regions: the auditory cortex and the visual cortex. The BOLD response in the auditory cortex was stronger during stimulation at hearable frequencies (20 and 100 Hz) whereas the response in the visual cortex was suppressed at infrasonic frequencies (3 Hz). Regardless of which hand was stimulated, the frequency-dependent effects were lateralized to the left auditory cortex and the right visual cortex. Furthermore, the frequency-dependent effects in both areas were abolished when the participants performed a visual task while receiving identical tactile stimulation as in the tactile threshold-tracking task. We interpret these findings in the context of the metamodal theory of brain function, which posits that brain areas contribute to sensory processing by performing specific computations regardless of input modality.

  • 4.
    Omrani, Mohsen
    et al.
    Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.
    Pruszynski, J. Andrew
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology. Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.
    Murnaghan, Chantelle D.
    Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada.
    Scott, Stephen H.
    Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada ; Department of Biomedical and Molecular Sciences, Kingston, Ontario, Canada ; Department of Medicine Queen's University, Kingston, Ontario, Canada.
    Perturbation-evoked responses in primary motor cortex are modulated by behavioral context2014In: Journal of Neurophysiology, ISSN 0022-3077, E-ISSN 1522-1598, Vol. 112, no 11, p. 2985-3000Article in journal (Refereed)
    Abstract [en]

    Corrective responses to external perturbations are sensitive to the behavioral task being performed. It is believed that primary motor cortex (M1) forms part of a transcortical pathway that contributes to this sensitivity. Previous work has identified two distinct phases in the perturbation response of M1 neurons, an initial response starting similar to 20 ms after perturbation onset that does not depend on the intended motor action and a task- dependent response that begins similar to 40 ms after perturbation onset. However, this invariant initial response may reflect ongoing postural control or a task- independent response to the perturbation. The present study tested these two possibilities by examining if being engaged in an ongoing postural task before perturbation onset modulated the initial perturbation response in M1. Specifically, mechanical perturbations were applied to the shoulder and/ or elbow while the monkey maintained its hand at a central target or when it was watching a movie and not required to respond to the perturbation. As expected, corrective movements, muscle stretch responses, and M1 population activity in the late perturbation epoch were all significantly diminished in the movie task. Strikingly, initial perturbation responses (<40 ms postperturbation) remained the same across tasks, suggesting that the initial phase of M1 activity constitutes a task- independent response that is sensitive to the properties of the mechanical perturbation but not the goal of the ongoing motor task.

  • 5. Pruszynski, J Andrew
    Primary motor cortex and fast feedback responses to mechanical perturbations: a primer on what we know now and some suggestions on what we should find out next.2014In: Frontiers in Integrative Neuroscience, ISSN 1662-5145, E-ISSN 1662-5145, Vol. 8Article in journal (Refereed)
    Abstract [en]

    Many researchers have drawn a clear distinction between fast feedback responses to mechanical perturbations (e.g., stretch responses) and voluntary control processes. But this simple distinction is difficult to reconcile with growing evidence that long-latency stretch responses share most of the defining capabilities of voluntary control. My general view-and I believe a growing consensus-is that the functional similarities between long-latency stretch responses and voluntary control processes can be readily understood based on their shared neural circuitry, especially a transcortical pathway through primary motor cortex. Here I provide a very brief and selective account of the human and monkey studies linking a transcortical pathway through primary motor cortex to the generation and functional sophistication of the long-latency stretch response. I then lay out some of the notable issues that are ready to be answered.

  • 6.
    Pruszynski, J. Andrew
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Department of Physiology and Pharmacology; Department of Psychology; Robarts Research Institute; Brain and Mind Institute, Western University, London, Canada.
    Flanagan, J. Randall
    Johansson, Roland S.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Fast and accurate edge orientation processing during object manipulation2018In: eLIFE, E-ISSN 2050-084X, Vol. 7, article id e31200Article in journal (Refereed)
    Abstract [en]

    Quickly and accurately extracting information about a touched object’s orientation is a critical aspect of dexterous object manipulation. However, the speed and acuity of tactile edge orientation processing with respect to the fingertips as reported in previous perceptual studies appear inadequate in these respects. Here we directly establish the tactile system’s capacity to process edge-orientation information during dexterous manipulation. Participants extracted tactile information about edge orientation very quickly, using it within 200 ms of first touching the object. Participants were also strikingly accurate. With edges spanning the entire fingertip, edge-orientation resolution was better than 3° in our object manipulation task, which is several times better than reported in previous perceptual studies. Performance remained impressive even with edges as short as 2 mm, consistent with our ability to precisely manipulate very small objects. Taken together, our results radically redefine the spatial processing capacity of the tactile system.

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  • 7.
    Pruszynski, J Andrew
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Johansson, Roland S
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology.
    Edge-orientation processing in first-order tactile neurons2014In: Nature Neuroscience, ISSN 1097-6256, E-ISSN 1546-1726, Vol. 17, no 10, p. 1404-1409Article in journal (Refereed)
    Abstract [en]

    A fundamental feature of first-order neurons in the tactile system is that their distal axon branches in the skin and forms many transduction sites, yielding complex receptive fields with many highly sensitive zones. We found that this arrangement constitutes a peripheral neural mechanism that allows individual neurons to signal geometric features of touched objects. Specifically, we observed that two types of first-order tactile neurons that densely innervate the glabrous skin of the human fingertips signaled edge orientation via both the intensity and the temporal structure of their responses. Moreover, we found that the spatial layout of a neuron's highly sensitive zones predicted its sensitivity to particular edge orientations. We submit that peripheral neurons in the touch-processing pathway, as with peripheral neurons in the visual-processing pathway, perform feature extraction computations that are typically attributed to neurons in the cerebral cortex.

  • 8.
    Pruszynski, J. Andrew
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Department of Physiology and Pharmacology, Department of Psychology, Robarts Research Institute, Brain and Mind Institute, Western University, London.
    Johansson, Roland S.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB).
    Flanagan, J. Randall
    A Rapid Tactile-Motor Reflex Automatically Guides Reaching toward Handheld Objects2016In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 26, no 6, p. 788-792Article in journal (Refereed)
    Abstract [en]

    The ability to respond quickly and effectively when objects in the world suddenly change position is essential for skilled action, and previous work has documented how unexpected changes in the location of a visually presented target during reaching can elicit rapid reflexive (i.e., automatic) corrections of the hand's trajectory [1-12]. In object manipulation and tool use, the sense of touch can also provide information about changes in the location of reach targets. Consider the many tasks where we reach with one hand to part of an object grasped by the other hand: reaching to a berry while holding a branch, reaching for a cap while grasping a bottle, and reaching toward a dog's collar while holding the dog's leash. In such cases, changes in the position of the reach target, due to wind, slip, or an active agent, can be detected, in principle, through touch. Here, we show that when people reach with their right hand to a target attached to the far end of a rod contacted, at the near end, by their left hand, an unexpected change in target location caused by rod rotation rapidly evokes an effective reach correction. That is, spatial information about a change in target location provided by tactile inputs to one hand elicits a rapid correction of the other hand's trajectory. In addition to uncovering a tactile-motor reflex that can support manipulatory actions, our results demonstrate that automatic reach corrections to moving targets are not unique to visually registered changes in target location.

  • 9.
    Pruszynski, J. Andrew
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology. Queen’s University, Kingston, Ontario.
    Kurtzer, Isaac
    New York College of Osteopathic Medicine, Queen’s University, Kingston, Ontario, New York College of Osteopathic Medicine, Old Westbury, New York.
    Nashed, Joseph Y.
    Queen’s University, Kingston, Ontario.
    Omrani, Mohsen
    Queen’s University, Kingston, Ontario.
    Brouwer, Brenda
    Queen’s University, Kingston, Ontario.
    Scott, Stephen H.
    Queen’s University, Kingston, Ontario.
    Primary motor cortex underlies multi-joint integration for fast feedback control2011In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 478, no 7369, p. 387-390Article in journal (Refereed)
    Abstract [en]

    A basic difficulty for the nervous system is integrating locally ambiguous sensory information to form accurate perceptions about the outside world(1-4). This local-to-global problem is also fundamental to motor control of the arm, because complex mechanical interactions between shoulder and elbow allow a particular amount of motion at one joint to arise from an infinite combination of shoulder and elbow torques(5). Here we show, in humans and rhesus monkeys, that a transcortical pathway through primary motor cortex (M1) resolves this ambiguity during fast feedback control. We demonstrate that single M1 neurons of behaving monkeys can integrate shoulder and elbow motion information into motor commands that appropriately counter the underlying torque within about 50 milliseconds of a mechanical perturbation. Moreover, we reveal a causal link between M1 processing and multi-joint integration in humans by showing that shoulder muscle responses occurring 50 milliseconds after pure elbow displacement can be potentiated by transcranial magnetic stimulation. Taken together, our results show that transcortical processing through M1 permits feedback responses to express a level of sophistication that rivals voluntary control; this provides neurophysiological support for influential theories positing that voluntary movement is generated by the intelligent manipulation of sensory feedback(6,7).

  • 10.
    Pruszynski, J Andrew
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology. Centre for Neuroscience Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada.
    Omrani, Mohsen
    Centre for Neuroscience Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada.
    Scott, Stephen H
    Centre for Neuroscience Studies, Departments of Biomedical and Molecular Sciences, and Medicine, Queen's University, Kingston, Ontario K7L 3N6, Canada.
    Goal-dependent modulation of fast feedback responses in primary motor cortex2014In: Journal of Neuroscience, ISSN 0270-6474, E-ISSN 1529-2401, Vol. 34, no 13, p. 4608-4617Article in journal (Refereed)
    Abstract [en]

    Many human studies have demonstrated that rapid motor responses (i.e., muscle-stretch reflexes) to mechanical perturbations can be modified by a participant's intended response. Here, we used a novel experimental paradigm to investigate the neural mechanisms that underlie such goal-dependent modulation. Two monkeys positioned their hand in a central area against a constant load and responded to mechanical perturbations by quickly placing their hand into visually defined spatial targets. The perturbation was chosen to excite a particular proximal arm muscle or isolated neuron in primary motor cortex and two targets were placed so that the hand was pushed away from one target (OUT target) and toward the other (IN target). We chose these targets because they produced behavioral responses analogous to the classical verbal instructions used in human studies. A third centrally located target was used to examine responses with a constant goal. Arm muscles and neurons robustly responded to the perturbation and showed clear goal-dependent responses ∼35 and 70 ms after perturbation onset, respectively. Most M1 neurons and all muscles displayed larger perturbation-related responses for the OUT target than the IN target. However, a substantial number of M1 neurons showed more complex patterns of target-dependent modulation not seen in muscles, including greater activity for the IN target than the OUT target, and changes in target preference over time. Together, our results reveal complex goal-dependent modulation of fast feedback responses in M1 that are present early enough to account for goal-dependent stretch responses in arm muscles.

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  • 11.
    Pruszynski, J. Andrew
    et al.
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB), Physiology. Queen’s University, Kingston.
    Scott, Stephen H.
    Queen’s University, Kingston.
    Optimal feedback control and the long-latency stretch response2012In: Experimental Brain Research, ISSN 0014-4819, E-ISSN 1432-1106, Vol. 218, no 3, p. 341-359Article, review/survey (Refereed)
    Abstract [en]

    There has traditionally been a separation between voluntary control processes and the fast feedback responses which follow mechanical perturbations (i.e., stretch "reflexes"). However, a recent theory of motor control, based on optimal control, suggests that voluntary motor behavior involves the sophisticated manipulation of sensory feedback. We have recently proposed that one implication of this theory is that the long-latency stretch "reflex", like voluntary control, should support a rich assortment of behaviors because these two processes are intimately linked through shared neural circuitry including primary motor cortex. In this review, we first describe the basic principles of optimal feedback control related to voluntary motor behavior. We then explore the functional properties of upper-limb stretch responses, with a focus on how the sophistication of the long-latency stretch response rivals voluntary control. And last, we describe the neural circuitry that underlies the long-latency stretch response and detail the evidence that primary motor cortex participates in sophisticated feedback responses to mechanical perturbations.

  • 12. Weiler, Jeffrey
    et al.
    Saravanamuttu, James
    Gribble, Paul L.
    Pruszynski, J. Andrew
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Brain and Mind Institute, Western University, London, Ontario, Canada; Department of Psychology, Western University, London, Ontario, Canada; Department of Physiology and Pharmacology, Western University, London, Ontario, Canada; Robarts Research Institute, Western University, London, Ontario, Canada.
    Coordinating long-latency stretch responses across the shoulder, elbow, and wrist during goal-directed reaching2016In: Journal of Neurophysiology, ISSN 0022-3077, E-ISSN 1522-1598, Vol. 116, no 5, p. 2236-2249Article in journal (Refereed)
    Abstract [en]

    The long-latency stretch response (muscle activity 50-100 ms after a mechanical perturbation) can be coordinated across multiple joints to support goal-directed actions. Here we assessed the flexibility of such coordination and whether it serves to counteract intersegmental dynamics and exploit kinematic redundancy. In three experiments, participants made planar reaches to visual targets after elbow perturbations and we assessed the coordination of long-latency stretch responses across shoulder, elbow, and wrist muscles. Importantly, targets were placed such that elbow and wrist (but not shoulder) rotations could help transport the hand to the target-a simple form of kinematic redundancy. In experiment 1 we applied perturbations of different magnitudes to the elbow and found that long-latency stretch responses in shoulder, elbow, and wrist muscles scaled with perturbation magnitude. In experiment 2 we examined the trial-by-trial relationship between long-latency stretch responses at adjacent joints and found that the magnitudes of the responses in shoulder and elbow muscles, as well as elbow and wrist muscles, were positively correlated. In experiment 3 we explicitly instructed participants how to use their wrist to move their hand to the target after the perturbation. We found that long-latency stretch responses in wrist muscles were not sensitive to our instructions, despite the fact that participants incorporated these instructions into their voluntary behavior. Taken together, our results indicate that, during reaching, the coordination of long-latency stretch responses across multiple joints counteracts intersegmental dynamics but may not be able to exploit kinematic redundancy.

  • 13. Zhao, Charlie W.
    et al.
    Daley, Mark J.
    Pruszynski, J. Andrew
    Umeå University, Faculty of Medicine, Department of Integrative Medical Biology (IMB). Dept. of Computer Science, Western University, London, Ontario, Canada; Brain and Mind Institute, Western University, London, Ontario, Canada; Dept. of Physiology and Pharmacology, Western University, London, Ontario, Canada; Dept. of Psychology, Western University, London, Ontario, Canada; Robarts Research Institute, Western University, London, Ontario, Canada.
    Neural network models of the tactile system develop first-order units with spatially complex receptive fields2018In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 6, article id e0199196Article in journal (Refereed)
    Abstract [en]

    First-order tactile neurons have spatially complex receptive fields. Here we use machine-learning tools to show that such complexity arises for a wide range of training sets and network architectures. Moreover, we demonstrate that this complexity benefits network performance, especially on more difficult tasks and in the presence of noise. Our work suggests that spatially complex receptive fields are normatively good given the biological constraints of the tactile periphery.

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