Anatomical and functional characterization of neuropil in the gracile fasciculus

A fundamental organizational principle of the central nervous system is that gray matter is the province of neuronal somata, white matter their processes. However, the rat and primate dorsal columns (archetypal spinal "white matter" tracts) are actually of intermediate character, insofar as they contain a surprisingly prominent neuropil of unknown function. Here I report on the morphology, inputs, projections, and functional properties of these neurons. Small fusiform and larger lentiform neurons are most abundant in the gracile fasciculus of the cervical and lumbar enlargements and are absent from the cuneate fasciculus and corticospinal tract. Many have dendrites that run along the dorsal pia, and, although in transverse sections these neurons appear isolated from the gray matter, they are also connected to area X by varicose and sometimes loosely fasciculated dendrites. These neurons receive neurochemically diverse, compartmentalized synaptic inputs (primary afferent, intrinsic and descending), half express the substance P receptor, and some project supraspinally. Unlike substantia gelatinosa neurons, they do not express protein kinase C gamma. Functionally, they have small receptive fields, which are somatotopically appropriate with respect to their anterior-posterior position along the neuraxis. They respond to innocuous and/or noxious mechanical stimulation of the distal extremities, and some are prone to central sensitization or "windup." Morphologically, neurochemically, and functionally, therefore, these cells most closely resemble neurons in laminae III-VI in the dorsal horn. The proximity of their dorsal dendrites to the pia mater may also reflect an ability to integrate internal (e.g., changes in cerebrospinal fluid compostition) and external (e.g., somatic) stimuli.