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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. The processing of proprioceptive signals in distributed networks: insights from insect motor control

   https://doi.org/10.1242/jeb.246182  

   Gebehart, Corinna; Büschges, Ansgar (January 2024, Journal of Experimental Biology)

   ABSTRACT The integration of sensory information is required to maintain body posture and to generate robust yet flexible locomotion through unpredictable environments. To anticipate required adaptations in limb posture and enable compensation of sudden perturbations, an animal's nervous system assembles external (exteroception) and internal (proprioception) cues. Coherent neuronal representations of the proprioceptive context of the body and the appendages arise from the concerted action of multiple sense organs monitoring body kinetics and kinematics. This multimodal proprioceptive information, together with exteroceptive signals and brain-derived descending motor commands, converges onto premotor networks – i.e. the local neuronal circuitry controlling motor output and movements – within the ventral nerve cord (VNC), the insect equivalent of the vertebrate spinal cord. This Review summarizes existing knowledge and recent advances in understanding how local premotor networks in the VNC use convergent information to generate contextually appropriate activity, focusing on the example of posture control. We compare the role and advantages of distributed sensory processing over dedicated neuronal pathways, and the challenges of multimodal integration in distributed networks. We discuss how the gain of distributed networks may be tuned to enable the behavioral repertoire of these systems, and argue that insect premotor networks might compensate for their limited neuronal population size by, in comparison to vertebrate networks, relying more heavily on the specificity of their connections. At a time in which connectomics and physiological recording techniques enable anatomical and functional circuit dissection at an unprecedented resolution, insect motor systems offer unique opportunities to identify the mechanisms underlying multimodal integration for flexible motor control. 

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3. Increase in weighting of vision vs. proprioception associated with force field adaptation

   https://doi.org/10.1038/s41598-019-46625-7  

   Sexton, Brandon M.; Liu, Yang; Block, Hannah J. (July 2019, Scientific Reports)

   Abstract Hand position can be estimated by vision and proprioception (position sense). The brain is thought to weight and integrate these percepts to form a multisensory estimate of hand position with which to guide movement. Force field adaptation, a type of cerebellum-dependent motor learning, is associated with both motor and proprioceptive changes. The cerebellum has connections with multisensory parietal regions; however, it is unknown if force adaptation is associated with changes in multisensory perception. If force adaptation affects all relevant sensory modalities similarly, the brain’s weighting of vision vs. proprioception should be maintained. Alternatively, if force perturbation is interpreted as somatosensory unreliability, vision may be up-weighted relative to proprioception. We assessed visuo-proprioceptive weighting with a perceptual estimation task before and after subjects performed straight-ahead reaches grasping a robotic manipulandum. Each subject performed one session with a clockwise or counter-clockwise velocity-dependent force field, and one session in a null field. Subjects increased their weight of vision vs. proprioception in the force field session relative to the null session, regardless of force field direction, in the straight-ahead dimension (F_1,44 = 5.13, p = 0.029). This suggests that force field adaptation is associated with an increase in the brain’s weighting of vision vs. proprioception. 

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4. 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)

   Synopsis 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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5. Organization of an ascending circuit that conveys flight motor state in Drosophila

   https://doi.org/10.1016/j.cub.2024.01.071  

   Cheong, Han S.J.; Boone, Kaitlyn N.; Bennett, Marryn M.; Salman, Farzaan; Ralston, Jacob D.; Hatch, Kaleb; Allen, Raven F.; Phelps, Alec M.; Cook, Andrew P.; Phelps, Jasper S.; et al (March 2024, Current Biology)

   Natural behaviors are a coordinated symphony of motor acts that drive reafferent (self-induced) sensory activation. Individual sensors cannot disambiguate exafferent (externally induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to carry out adaptive behaviors through corollary discharge circuits (CDCs), which provide predictive motor signals from motor pathways to sensory processing and other motor pathways. Yet, how CDCs comprehensively integrate into the nervous system remains unexplored. Here, we use connectomics, neuroanatomical, physiological, and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs) in Drosophila, which function as a predictive CDC in other insects. Both AHN pairs receive input primarily from a partially overlapping population of descending neurons, especially from DNg02, which controls wing motor output. Using Ca2+ imaging and behavioral recordings, we show that AHN activation is correlated to flight behavior and precedes wing motion. Optogenetic activation of DNg02 is sufficient to activate AHNs, indicating that AHNs are activated by descending commands in advance of behavior and not as a consequence of sensory input. Downstream, each AHN pair targets predominantly non-overlapping networks, including those that process visual, auditory, and mechanosensory information, as well as networks controlling wing, haltere, and leg sensorimotor control. These results support the conclusion that the AHNs provide a predictive motor signal about wing motor state to mostly non-overlapping sensory and motor networks. Future work will determine how AHN signaling is driven by other descending neurons and interpreted by AHN downstream targets to maintain adaptive sensorimotor performance. 

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