Physiology and Morphology of Shared and Specialized Spinal Interneurons for Locomotion and Scratching

Abstract

Berkowitz A. Physiology and morphology of shared and specialized spinal interneurons for locomotion and scratching. J Neurophysiol 99: 2887-2901, 2008. First published April 2, 2008 doi:10.1152/jn.90235.2008. Distinct types of rhythmic movements that use the same muscles are typically generated largely by shared multifunctional neurons in invertebrates, but less is known for vertebrates. Evidence suggests that locomotion and scratching are produced partly by shared spinal cord interneuronal circuity, although direct evidence with intracellular recording has been lacking. Here, spinal interneurons were recorded intracellularly during fictive swimming and fictive scratching in vivo and filled with Neurobiotin. Some interneurons that were rhythmically activated during both swimming and scratching had axon terminal arborizations in the ventral horn of the hindlimb enlargement, indicating their likely contribution to hindlimb motor outputs during both behaviors. We previously described a morphological group of spinal interneurons ("transverse interneurons" or T neurons) that were rhythmically activated during all forms of fictive scratching at higher peak firing rates and with larger membrane potential oscillations than scratch-activated spinal interneurons with different dendritic orientations. The current study demonstrates that T neurons are activated during both swimming and scratching and thus are components of the shared circuitry. Many spinal interneurons activated during fictive scratching are also activated during fictive swimming (scratch/swim neurons), but others are suppressed during swimming (scratch-specialized neurons). The current study demonstrates that some scratch-specialized neurons receive strong and long-lasting hyperpolarizing inhibition during fictive swimming and are also morphologically distinct from T neurons. Thus this study indicates that locomotion and scratching are produced by a combination of shared and dedicated interneurons whose physiological and morphological properties are beginning to be revealed.

A Neural Basis for Motor Primitives in the Spinal Cord

“…However, the population average response included some neurons that fired strongly around the onsets (or early in bursting) of primitives and some after termination. This is similar to some neurons from Berkowitz's intracellular data (Berkowitz, 2008) and to Stein's OFF and ON units (Stein, 2008).…”

“…Nonetheless, close but qualified correspondences exist. Berkowitz (2005Berkowitz ( , 2006Berkowitz ( , 2008 found shared neurons deeper in gray. Many of these neurons were recruited across many behaviors in the turtle.…”

“…As noted by Berkowitz (2008), both shared and dedicated neurons contribute to multiple motor behaviors in most invertebrates. Examination of both extracellular and intracellular recordings in turtle fictive and nonfictive preparations by Stein, Berkowitz, Currie, Hounsgaard, and others also show both shared and dedicated neurons recruited in fictive vertebrate motor patterns (Berkowitz, 2001(Berkowitz, , 2002(Berkowitz, , 2008Alaburda et al, 2005;Stein, 2005Stein, , 2008Berg et al, 2007;Samara and Currie, 2008).…”

“…We found a subset of 46 cells in intermediate gray in which STA identified short-latency postspike facilitations indicating functional monosynaptic, disynaptic, or perhaps trisynaptic connections to motor pools. Like Berkowitz's (2008) intracellular study in turtle, these interneurons would be reused across behaviors, reflecting the activation of the same motor pattern in multiple contexts. Berkowitz showed direct anatomical projections of such reused neurons into the motor pools.…”

Stereological Estimate of the Total Number of Neurons in Spinal Segment D9 of the Red-Eared Turtle

“…Using the scratch circuit in the spinal cord of the adult turtle as a model network, the present study provides insight into both these aspects. Segment D9 in the turtle is an integral part of the lumbar network for scratch and swim movements (Berkowitz, 2008). The stereological counting procedure was verified by comparing the estimated average number of MN (2049) in segment D9 to the number of myelinated fibers in the segmental ventral roots (2114).…”