Rapid shifts in receptive fields of cells in trigeminal subnucleus interpolaris following infraorbital nerve transection in adult rats

Abstract

Transection of the infraorbital nerve in adult rats results in an array of chronic functional anomalies in trigeminal brainstem subnucleus interpolaris, including changes in normal receptive field organization. This work examined whether long-term maintenance of acute modifications, such as unmasking or strengthening of normally ineffective inputs to interpolaris cells, might contribute to the previously described chronic abnormalities. Using glass micropipettes, extracellular isolation of 37 interpolaris cells, with infraorbital receptive fields, was maintained following intraorbital transection of the infraorbital nerve. Receptive fields and dynamic response properties were characterized immediately before and after the cut and throughout the post-transection isolation period. Orthodromic latencies to trigeminal ganglion shocks and antidromic activation from thalamus or cerebellum were also examined. Of the 37 cells, 21.6% exhibited receptive field shifts to non-infraorbital regions after cutting the infraorbital nerve. Using the normal probability of observing an interpolaris cell with more than one trigeminal division in its receptive field, the probability of observing this shift by chance was 0.0013. No such changes were observed for 12 control cells, recorded for durations equal to or greater than total recording times for the shifting cells, with the nerve intact. The representation of local circuit, thalamic-projecting and cerebellar-projecting cells was similar in the total sample; however, all neurons exhibiting transection-induced receptive field shifts were projection neurons. In comparing the sample of cells that exhibited receptive field shifts with those that did not, prior to infraorbital nerve cut, there was no difference in mean latencies and thresholds for activation from the stimulating electrodes or in mean depth at which the cells were isolated. In addition, no difference was evident in receptive field size, effective receptor surface, dynamic response characteristics or spontaneous activity. These data suggest that maintenance of acute receptive field changes, following infraorbital nerve cut, may contribute to some types of chronic functional alterations observed after such damage.