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1. Corollary discharge prevents signal distortion and enhances sensing during locomotion

   https://doi.org/10.1101/2021.02.15.431323  

   Skandalis, * ; Lunsford, Elias T. ; Liao*, James C. ( February 2021 , bioRxiv)

   null (Ed.)

   Sensory feedback during movement entails sensing a mix of externally- and self-generated stimuli (respectively, exafference and reafference). In many peripheral sensory systems, a parallel copy of the motor command, a corollary discharge, is thought to eliminate sensory feedback during behaviors. However, reafference has important roles in motor control, because it provides real-time feedback on the animal’s motions through the environment. In this case, the corollary discharge must be calibrated to enable feedback while avoiding negative consequences like sensor fatigue. The undulatory motions of fishes’ bodies generate induced flows that are sensed by the lateral line sensory organ, and prior work has shown these reafferent signals contribute to the regulation of swimming kinematics. Corollary discharge to the lateral line reduces the gain for reafference, but cannot eliminate it altogether. We develop a data-driven model integrating swimming biomechanics, hair cell physiology, and corollary discharge to understand how sensory modulation is calibrated during locomotion in larval zebrafish. In the absence of corollary discharge, lateral line afferent units exhibit the highly heterogeneous habituation rates characteristic of hair cell systems, typified by decaying sensitivity and phase distortions with respect to an input stimulus. Activation of the corollary discharge prevents habituation, reduces response heterogeneity, and regulates response phases in a narrow interval around the time of the peak stimulus. This suggests a synergistic interaction between the corollary discharge and the polarization of lateral line sensors, which sharpens sensitivity along their preferred axes. Our integrative model reveals a vital role of corollary discharge for ensuring precise feedback, including proprioception, during undulatory locomotion. 

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2. Mechanistic Hypotheses for Proprioceptive Sensing Within the Avian Lumbosacral Spinal Cord

   https://doi.org/10.1093/icb/icad052  

   Stanchak, Kathryn E. ; Miller, Kimberly E. ; Shikiar, Devany ; Brunton, Bingni W. ; Perkel, David J. ( June 2023 , Integrative And Comparative Biology)

   Animals need to accurately sense changes in their body position to perform complex movements. It is increasingly clear that the vertebrate central nervous system contains a variety of cells capable of detecting body motion, in addition to the comparatively well-understood mechanosensory cells of the vestibular system and the peripheral proprioceptors. One such intriguing system is the lower spinal cord and column in birds, also known as the avian lumbosacral organ (LSO), which is thought to act as a set of balance sensors that allow birds to detect body movements separately from head movements detected by the vestibular system. Here, we take what is known about proprioceptive, mechanosensory spinal neurons in other vertebrates to explore hypotheses for how the LSO might sense mechanical information related to movement. Although the LSO is found only in birds, recent immunohistochemical studies of the avian LSO have hinted at similarities between cells in the LSO and the known spinal proprioceptors in other vertebrates. In addition to describing possible connections between avian spinal anatomy and recent findings on spinal proprioception as well as sensory and sensorimotor spinal networks, we also present some new data that suggest a role for sensory afferent peptides in LSO function. Thus, this perspective articulates a set of testable ideas on mechanisms of LSO function grounded in the emerging spinal proprioception scientific literature.

    

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3. Somatosensory changes associated with motor skill learning

   https://doi.org/10.1152/jn.00497.2019  

   Mirdamadi, Jasmine Lauren ; Block, Hannah J ( January 2020 , Journal of Neurophysiology)

   Trial-and-error motor adaptation has been linked to somatosensory plasticity and shifts in proprioception (limb position sense). The role of sensory processing in motor skill learning is less understood. Unlike adaptation, skill learning involves the acquisition of new movement patterns in the absence of perturbation, with performance limited by the speed-accuracy tradeoff. We investigated somatosensory changes during motor skill learning at the behavioral and neurophysiological level. Twenty-eight healthy young adults practiced a maze-tracing task, guiding a robotic manipulandum through an irregular 2D track featuring several abrupt turns. Practice occurred on days 1 and 2. Skill was assessed before practice on day 1 and again on day 3, with learning indicated by a shift in the speed-accuracy function between these assessments. Proprioceptive function was quantified with a passive two-alternative forced choice task. In a subset of 15 participants, we measured short latency afferent inhibition (SAI) to index somatosensory projections to motor cortex. We found that motor practice enhanced the speed-accuracy skill function (F 4,108 = 32.15, p < 0.001) and was associated with improved proprioceptive sensitivity at retention (t 22 = 24.75, p = 0.0031). Further, SAI increased after training (F 1,14 = 5.41, p = 0.036). Interestingly, individuals with larger increases in SAI, reflecting enhanced somatosensory afference to motor cortex, demonstrated larger improvements in motor skill learning. These findings suggest that SAI may be an important functional mechanism for some aspect of motor skill learning. Further research is needed to test what parameters (task complexity, practice time, etc) are specifically linked to somatosensory function. 

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4. Investigating the role of low level reinforcement reflex loops in insect locomotion

   https://doi.org/10.1088/1748-3190/ac28ea  

   Goldsmith, C A ; Quinn, R D ; Szczecinski, N S ( October 2021 , Bioinspiration & Biomimetics)

   Abstract Insects are highly capable walkers, but many questions remain regarding how the insect nervous system controls locomotion. One particular question is how information is communicated between the ‘lower level’ ventral nerve cord (VNC) and the ‘higher level’ head ganglia to facilitate control. In this work, we seek to explore this question by investigating how systems traditionally described as ‘positive feedback’ may initiate and maintain stepping in the VNC with limited information exchanged between lower and higher level centers. We focus on the ‘reflex reversal’ of the stick insect femur-tibia joint between a resistance reflex (RR) and an active reaction in response to joint flexion, as well as the activation of populations of descending dorsal median unpaired (desDUM) neurons from limb strain as our primary reflex loops. We present the development of a neuromechanical model of the stick insect ( Carausius morosus ) femur-tibia (FTi) and coxa-trochanter joint control networks ‘in-the-loop’ with a physical robotic limb. The control network generates motor commands for the robotic limb, whose motion and forces generate sensory feedback for the network. We based our network architecture on the anatomy of the non-spiking interneuron joint control network that controls the FTi joint, extrapolated network connectivity based on known muscle responses, and previously developed mechanisms to produce ‘sideways stepping’. Previous studies hypothesized that RR is enacted by selective inhibition of sensory afferents from the femoral chordotonal organ, but no study has tested this hypothesis with a model of an intact limb. We found that inhibiting the network’s flexion position and velocity afferents generated a reflex reversal in the robot limb’s FTi joint. We also explored the intact network’s ability to sustain steady locomotion on our test limb. Our results suggested that the reflex reversal and limb strain reinforcement mechanisms are both necessary but individually insufficient to produce and maintain rhythmic stepping in the limb, which can be initiated or halted by brief, transient descending signals. Removing portions of this feedback loop or creating a large enough disruption can halt stepping independent of the higher-level centers. We conclude by discussing why the nervous system might control motor output in this manner, as well as how to apply these findings to generalized nervous system understanding and improved robotic control. 

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5. Comparison of Proximal Leg Strain in Locomotor Model Organisms Using Robotic Legs

   Dinges, G.F. ; Zyhowski, W.P. ; Goldsmith, C.A. ; Szczecinski, N.S. ( August 2023 , Biomimetic and Biohybrid Systems. Living Machines 2023.)

   Meder, F. ; Hunt, A. ; Margheri, L. ; Mura, A. ; Mazzolai, B. (Ed.)

   Insects use various sensory organs to monitor proprioceptive and exteroceptive information during walking. The measurement of forces in the exoskeleton is facilitated by campaniform sensilla (CS), which monitor resisted muscle forces through the detection of exoskeletal strains. CS are commonly found in leg segments arranged in fields, groups, or as single units. Most insects have the highest density of sensor locations on the trochanter, a proximal leg segment. CS are arranged homologously across species, suggesting comparable functions despite noted morphological differences. Furthermore, the trochanter–femur joint is mobile in some species and fused in others. To investigate how different morphological arrangements influence strain sensing in different insect species, we utilized two robotic models of the legs of the fruit fly Drosophila melanogaster and the stick insect Carausius morosus. Both insect species are past and present model organisms for unraveling aspects of motor control, thus providing extensive information on sensor morphology and, in-part, function. The robotic models were dynamically scaled to the legs of the insects, with strain gauges placed with correct orientations according to published data. Strains were detected during stepping on a treadmill, and the sensor locations and leg morphology played noticeable roles in the strains that were measured. Moreover, the sensor locations that were absent in one species relative to the other measured strains that were also being measured by the existing sensors. These findings contributed to our understanding of load sensing in animal locomotion and the relevance of sensory organ morphology in motor control. 

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