Molecular markers of mechanosensation in glycinergic neurons in the avian lumbosacral spinal cord

Abstract

Birds are exceptionally adept at controlling their body position. For example, they can coordinate rapid movements of their body while stabilizing their head. Intriguingly, this ability may rely in part on a mechanosensory organ in the avian lower spinal cord called the lumbosacral organ (LSO). However, molecular mechanotransduction mechanisms have not been identified in the avian spinal cord. Here, we report the presence of glycinergic neurons in the LSO that exhibit immunoreactivity for myosin7a and espin, molecules essential for function and maintenance of hair cells in the inner ear. Specifically, we find glycinergic cell bodies near the central canal and processes that extend laterally to the accessory lobes and spinal ligaments. These LSO neurons are reminiscent of glycinergic neurons in a recently-described lateral spinal proprioceptive organ in zebrafish that detects spinal bending. The avian LSO, however, is located inside a series of fused vertebrae called the synsacrum, which constrains spinal bending. We suggest the LSO may be a modification and elaboration of a pre-existing mechanosensory spinal network in vertebrates. A mechanistic understanding of its function may be an important clue to understanding the evolution and development of avian locomotion.

Significance Statement

The spinal cord can help control posture by sensing bending of the spinal column. In birds, the lower spinal column is fused and cannot bend. Notably, this region of the avian spinal cord has several specialized features compared with other vertebrates. We report neurons in the lower bird spinal cord that express proteins known to be involved in sensing mechanical signals. These neurons share characteristics of other spinal cord mechanosensory cells. This suggests that spinal cords across vertebrates are capable of mechanosensation and that spinal mechanosensory networks have evolved to allow unique functions, such as in the constrained lower spinal cord of birds. These data provide an avenue for molecular manipulations of these cells, permitting experimental tests of their role in controlling posture.