Somatotopic organization of the different functional types of trigeminal ganglion neurons innervating the ocular surface and periocular tissues

Abstract

Purpose : To determine whether the different functional types of sensory neurons innervating the eye and the periocular tissues are somatotopically organized within the trigeminal ganglion (TG).

Methods : Anesthetized adult male Wistar rats were placed in a stereotaxic frame. Neuronal activity within the right TG was recorded extracellularly with tungsten electrodes (2-5MΩ). A 0.5mm resolution XY grid was defined (-1.0 to -3.0mm lateral to bregma; 0.0 to -3.0 mm posterior to bregma) to define the stereotaxic coordinates of each recorded neuron. Depth (in µm) within the TG was also measured. For each of the recorded TG neurons (n=150), receptive field (RF) was mapped using mechanical (wet fine paint brush) or cold stimuli (0.5mm-diameter ice-cooled metal probe). Response to chemical stimulation (100µM menthol; 98%CO₂ gas jets) was explored to check polymodality of the units. Neurons were classified depending on their sensory class and RF location (cornea, bulbar or tarsal conjunctiva, upper or lower eyelid borders), and the stereotaxic coordinates of each functional group along the antero-posterior, medio-lateral, and dorso-ventral axes were defined.

Results : The different functional types of neurons innervating the eye were situated preferentially in a defined area of the antero-medial TG (around -2.0/-1.5), the corneal ones were located more anteriorly than those innervating tarsal and bulbar conjunctiva (Figure 1). Neurons innervating the upper eyelid were positioned at XY coordinates similar to corneal neurons (Figure 1), but more dorsally (100µm depth) than neurons innervating the cornea (300µm depth).

Conclusions : The gross somatotopy described for the whole TG persists within the ophthalmic branch. This knowledge may help to target appropriate groups of neurons during in vivo studies examining the nerve activity underlying sensations referred to ocular and periocular tissues, such as discomfort and pain evoked by eye dryness and contact lens wearing and eventually to define more precisely eye sensation deficits caused by TG lesions.

This is an abstract that was submitted for the 2017 ARVO Annual Meeting, held in Baltimore, MD, May 7-11, 2017.

 

Figure 1. Contour plots showing the probability to find neurons with RF in a particular ocular or periocular area. Position relative to bregma (0.0/0.0 coordinate) is expressed in mm. Color coding presents the probability of finding in a particular ocular location the RF of neurons recorded in this coordinate.