Electrophysiological and morphological evidence for a diameter-based innervation pattern of the superior colliculus

Neurophysiological and morphological techniques were used to describe changes in the optic tract and superior colliculus (SC) in response to unilateral enucleation. Long-Evans, male (greater than 250 g) rats were implanted with chronic bipolar stimulating electrodes located in the optic chiasm and a recording electrode located below the stratum griseum superficiale (SGS) and referenced to a skull screw electrode. In rats with satisfactory electrode placements (n = 15), peaks corresponding to rapidly conducting presynaptic activity (Pre), rapidly conducting postsynaptic activity (N1), and slowly conducting postsynaptic activity (P3) were identified according to peak latency, polarity, stimulation threshold, and resistance to 100-Hz stimulation. These peaks diminished differentially over a 7 day (D1-7) postenucleation period. Those peaks reflecting rapidly conducting axons (i.e., Pre, N1) decayed by D2, whereas those reflecting slowly conducting axons (i.e., P3) persisted until D4 and decayed completely by D7. In a separate set of enucleated rats (n = 25), the progression of degeneration in the SC was outlined morphologically from D1-7 using both light and electron microscopy. Light microscopy of semithin epoxy sections indicated that degenerative changes, consisting largely of swollen axons and myelin debris, appeared first in the upper stratum opticum (SO) and lower SGS on D1,2, progressed upward throughout the middle SGS by D4, and finally involved the entire SGS and lower stratum zonale (SZ) by D5-7. Electron microscopy, however, indicated that although degenerated terminals were seen in the lower SGS, at (D1,2), the majority of degenerated synapses were restricted to the upper SGS at the later time points. Coupled with the electrophysiological data, these observations indicate that within the SGS, early degenerating, large diameter optic nerve fibers terminate below slower degenerating, smaller diameter fibers.