Somato-Dendritic Morphology Predicts Physiology for Neurons That Contribute to Several Kinds of Limb Movements

Abstract

Berkowitz, Ari, Gina L. C. Yosten, and R. Mark Ballard. Somatodendritic morphology predicts physiology for neurons that contribute to several kinds of limb movements. J Neurophysiol 95: 2821-2831, 2006. First published February 1, 2006 doi:10.1152/jn.01246.2005. It has been difficult to predict the behavioral roles of vertebrate CNS neurons based solely on their morphologies, especially for the neurons that control limb movements in adults. We examined the morphologies of spinal interneurons involved in limb movement control, using intracellular recording followed by Neurobiotin injection in the in vivo adult turtle spinal cord preparation. We report here the first description of a class of spinal interneurons whose somato-dendritic morphologies predict their robust activity during multiple forms of ipsilateral and contralateral fictive hindlimb scratching and fictive hindlimb withdrawal. These "transverse interneurons" or T cells have a mediolaterally elongated soma and a simple dendritic tree that is extensive in the transverse plane but restricted rostrocaudally. During fictive scratching, these cells display strong rhythmic modulation with higher peak firing rates than other scratch-activated interneurons. These higher peak firing rates are at least partly caused by T cells having larger phase-locked membrane potential oscillations and narrower action potentials with briefer afterhyperpolarizations than other scratch-activated interneurons. Many T cells have axon terminal arborizations in the ventral horn of the spinal cord hindlimb enlargement. Identification of this morphological and physiological class of spinal interneurons should facilitate further exploration of the mechanisms of hindlimb motor pattern selection and generation.

A Neural Basis for Motor Primitives in the Spinal Cord

“…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.…”

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

“…The group of T neurons (Berkowitz et al 2006) was defined (Fig. 1B) using two criteria, which were ratios of somatic and dendritic lengths along the three axes (rostrocaudal, R-…”

“…Statistical comparisons of mean peak firing rates and mean oscillation amplitudes were made using the Mann-Whitney test; in general, two-tailed tests were used, but for comparisons of firing rates and oscillation amplitudes between T neurons and non-T neurons, onetailed tests were used because there was prior evidence that T neurons have higher peak firing rates and larger oscillations than those of non-T neurons (Berkowitz et al 2006). To test for correlations of individual neuron parameters between scratching and swimming, Pearson's correlation coefficient (r) was used for linear parameters (MVL and oscillation amplitude), whereas the circular-circular correlation coefficient (r c ) (Batschelet 1981) was used for cyclical parameters (MVA and oscillation phase and trough).…”

“…Only in studies of tadpole (Li et al 2007;Soffe 1993) and fish (Kimura et al 2006) axial body movements, turtle hindlimb scratching and withdrawal (Berkowitz 2005;Berkowitz et al 2006), and mammalian eupneic breathing, sighing, coughing, and sneezing (Lieske et al 2000;Shiba et al 2007) have investigators recorded from individual interneurons while eliciting multiple types of naturalistic motor patterns and also assessed the axonal projections or synaptic targets of these cells. The issue of whether interneurons contribute to one or multiple types of movement is conveniently addressed using the turtle spinal cord, which can produce hindlimb motor patterns underlying forward swimming, three forms of scratching, and withdrawal without input from the brain and movement-related feedback (Stein 2005).…”

“…Recently, we defined a morphological group, transverse interneurons (T neurons), that are activated during all forms of scratching. They tend to have higher peak firing rates than those of other scratch-activated interneurons and can have axon terminals in the hindlimb enlargement ventral horn (Berkowitz et al 2006). It is not known, however, whether T neurons are activated during swimming.…”