Electrophysiological properties of identified trigeminal ganglion neurons innervating the cornea of the mouse

Abstract

The cornea is innervated by three functional types of neurons: mechanosensory, polymodal and cold-sensitive neurons, all of which are presumed to be nociceptive. To explore if corneal neurons constitute a heterogeneous population according to their electrophysiological properties, intracellular recordings were made in vitro from trigeminal ganglion neurons innervating the cornea of the mouse. Corneal neurons were labelled with FluoroGold applied after a corneal epithelial wound. Five days later, the trigeminal ganglion attached to the eye by its nerves was removed and placed in a superfusion chamber. FluoroGold-positive cells that also responded to electrical stimulation of the cornea were considered corneal neurons. Non-corneal neurons were also studied. Based on their conduction velocity at room temperature, corneal neurons were classified as myelinated A (>1.5m/s) or non-myelinated C (< or =1.5m/s) neurons. A and C neurons differed significantly in their passive and active electrical properties. Virtually all corneal C neurons and about two-thirds of A neurons exhibited a hump in the falling phase of the action potential (S neurons), while the remaining A neurons (F neurons) showed faster and narrower action potentials without a hump. Among non-corneal neurons, A neurons of the F type were found in a proportion of about 50%. Based on their ability to produce somatic action potentials in tetrodotoxin (0.1 microM), non-corneal neurons were classified as fully or partially tetrodotoxin sensitive, which were mainly of the Adelta type, and tetrodotoxin resistant, which were C neurons. Among the corneal neurons, those with a faster action potential, possibly associated to the expression of tetrodotoxin-sensitive Na(+) channels, may be pure corneal mechanosensory neurons, all of which are known to belong to the Adelta type. Neurons with a slower action potential showing a hump in the repolarization phase are both corneal Adelta and C polymodal nociceptive neurons, a type of cell in which tetrodotoxin-resistant Na(+) channels have been identified. The possibility is raised that the small population of neurons with a very high input resistance are cold-sensitive neurons. From the present results, we suggest that the electrophysiological properties of primary sensory neurons innervating the cornea are attributable not only to their conduction velocities, but also to the functional characteristics of their peripheral nerve terminals.