title: Musculoskeletal geometry accounts for apparent extrinsic representation of paw position in dorsal spinocerebellar tract.
abstract: Proprioception, the sense of limb position and motion, arises from individual muscle receptors. An important question is how and where in the neuroaxis our high level "extrinsic" sense of limb movement originates. In the 1990s, a series of papers detailed the properties of neurons in the dorsal spinocerebellar tract (DSCT) of the cat. Despite their direct projections from sensory receptors, it appeared that half of these neurons had consistent, high-level tuning to paw position rather than to joint angles (or muscle lengths). These results suggested that many DSCT neurons compute paw position from lower level sensory information. We examined the contribution of musculoskeletal geometry to this apparent extrinsic representation by simulating a three-joint hindlimb with mono- and biarticular muscles, each providing a muscle spindlelike signal, modulated by the muscle length. We simulated neurons driven by randomly weighted combinations of these signals and moved the paw to different positions under two joint-covariance conditions similar to the original experiments. Our results paralleled those experiments in a number of respects:1) Many neurons were tuned to paw position relative to the hip under both conditions.2) The distribution of tuning was strongly bimodal, with most neurons driven by whole-leg flexion or extension.3) The change in tuning between conditions clustered around zero (median absolute change ~20°). These results indicate that, at least for these constraint conditions, extrinsic-like representation can be achieved simply through musculoskeletal geometry and convergent muscle length inputs. Consequently, they suggest a reinterpretation of the earlier results may be required.NEW & NOTEWORTHYA classic experiment concluding that many dorsal spinocerebellar tract neurons encode paw position rather than joint angles has been cited by many studies as evidence for high-level computation occurring within a single synapse of the sensors. However, our study provides evidence that such a computation is not required to explain the results. Using simulation, we replicated many of the original results with purely random connectivity, suggesting that a reinterpretation of the classic experiment is needed.
authors.affiliation: Department of Biomedical Engineering, Northwestern University, Evanston, Illinois.
authors.forename: Raeed H
authors.identifier: 0000-0002-5934-919X
authors.initials: RH
authors.lastname: Chowdhury
authors.affiliation: Department of Biomedical Engineering, Northwestern University, Evanston, Illinois.|Department of Physiology, Northwestern University, Chicago, Illinois.|Department of Physical Medicine and Rehabilitation, Northwestern University and Rehabilitation Institute of Chicago, Chicago, Illinois; and.|Shirley Ryan AbilityLab, Chicago, Illinois.
authors.forename: Matthew C
authors.initials: MC
authors.lastname: Tresch
authors.affiliation: Department of Biomedical Engineering, Northwestern University, Evanston, Illinois; LM@northwestern.edu.|Department of Physiology, Northwestern University, Chicago, Illinois.|Department of Physical Medicine and Rehabilitation, Northwestern University and Rehabilitation Institute of Chicago, Chicago, Illinois; and.|Shirley Ryan AbilityLab, Chicago, Illinois.
authors.forename: Lee E
authors.identifier: 0000-0001-8675-7140
authors.initials: LE
authors.lastname: Miller
mesh_terms: D000818:Animals; D006614:Hindlimb / Q000294:innervation* / Q000502:physiology; D008959:Models, Neurological; D009068:Movement; D018482:Muscle, Skeletal / Q000294:innervation* / Q000502:physiology; D009474:Neurons / Q000502:physiology; D020824:Spinocerebellar Tracts / Q000166:cytology / Q000502:physiology*
keywords: biomechanics; cat hindlimb; dorsal spinocerebellar tract; proprioception; simulation