C-fiber depletion alters response properties of neurons in trigeminal nucleus principalis

The effects of C-fiber depletion induced by neonatal capsaicin treatment on the functional properties of vibrissa-sensitive low-threshold mechanorecep tive (LTM) neurons in the rat trigeminal nucleus principalis were examined in adult rats. Neonatal rats were injected either with capsaicin or its veh icle within 48 h of birth. The depletion of unmyelinated afferents was conf irmed by the significant decrease in plasma extravasation of Evan's blue dy e induced in the hindlimb skin of capsaicin-treated rats by cutaneous appli cation of mustard oil and by the significant decrease of unmyelinated fiber s in both the sciatic and infraorbital nerves. The mechanoreceptive field ( RF) and response properties of 31 vibrissa-sensitive neurons in capsaicin-t reated rats were compared with those of 32 vibrissa-sensitive neurons in co ntrol (untreated or vehicle-treated) rats. The use of electronically contro lled mechanical stimuli allowed quantitative analysis of response propertie s of vibrissa-sensitive neurons; these included the number of center- and s urround-RF vibrissae within the RF (i.e., those vibrissae which when stimul ated elicited greater than or equal to 1 and <1 action potential per stimul us, respectively), the response magnitude and latency, and the selectivity of responses to stimulation of vibrissae in different directions with empha sis on combining both the response magnitude and direction of vibrissal def lection in a vector analysis. Neonatal capsaicin treatment was associated w ith significant increases in the total number of vibrissae, in the number o f center-RF vibrissae per neuronal RF, and in the percentage of vibrissa-se nsitive neurons that also responded to stimulation of other types of orofac ial tissues. Compared with control rats, capsaicin-treated rats showed sign ificant increases in the response magnitude to stimulation of surround-RF v ibrissae as well as in response latency variability to stimulation of both center- and surround-RF vibrissae. C-fiber depletion also significantly alt ered the directional selectivity of responses to stimulation of vibrissae. For neurons with multiple center-RF vibrissae, the proportion of center-RF vibrissae with net vector responses oriented toward the same quadrant was s ignificantly less in capsaicin-treated compared with control rats. These ch anges in the functional properties of principalis vibrissa-sensitive neuron s associated with marked depletion of C-fiber afferents are consistent with similarly induced alterations in LTM neurons studied at other levels of th e rodent somatosensory system, and indeed may contribute to alterations pre viously described in the somatosensory cortex of adult rodents. Furthermore , these results provide additional support to the view that C fibers may ha ve an important role in shaping the functional properties of LTM neurons in central somatosensory pathways.