The effects of post-ganglionic axotomy on selective synaptic connexions in the superior cervical ganglion of the guinea-pig.

Stimulation of preganglionic axons arising from different levels of the thoracic spinal cord causes different effects on end-organs supplied by the superior cervical ganglion (Langley, 1892; Nja & Purves, 1977a; Lichtman, Purves & Yip, 1979). For example, stimulation of the first thoracic ventral root (T1) causes pupillary dilatation and widening of the palpebral fissure; stimulation of T4, on the other hand, has little effect on the eye, even though axons arising from this level innervate about as many superior cervical ganglion cells as those from T1. Thus ganglion cell innervation is selective. (1) Three months after crushing the major post-ganglionic branches of the superior cervical ganglion this differential effectiveness is lost: T1 and T4 stimulation have approximately equal effects on the end-organs of the eye. (2) In normal animals, the cellular counterpart of selective end-organ effects is the innervation of each ganglion cell by a contiguous subset of the spinal segments that innervate the ganglion as a whole. One of these segments is usually dominant, the strength of innervation from adjacent segments falling off as a function of distance from the dominant one (Nja & Purves, 1977a). Intracellular recordings from ganglion cells 3 months after post-ganglionic axotomy showed that this selective pattern is re-established. (3) Since the innervation of ganglion cells appears normal, the abnormal end-organ responses after post-ganglionic axotomy suggest that ganglion cell axons are not limited to their original targets during peripheral re-innervation. This suggestion is supported by the finding that ganglion cells sending axons to different peripheral destinations via the second and third cervical spinal nerves were no longer distinguishable on the basis of their segmented inputs 3 months after post-ganglionic axotomy. (4) Similar results were obtained when the preganglionic cervical trunk was cut at the same time as the post-ganglionic axons were crushed; the pattern of end-organ responses was abnormal, whereas individual ganglion cells were re-innervated according to the rules of contiguity and segmental dominance. (5) These results indicate that ganglion cells do not undergo a compensatory change in the segmental innervation they receive when their axons regenerate to targets different from, or in addition to those they originally innervated, even when an entirely new set of ganglionic connexions is formed. This suggests that ganglion cells, or some aspect of their immediate environment, possess a permanent label that determines the segmental innervation they receive.