Figure 11. Two alternative ways neural circuits could reach the mature state in a developing efferent pathway.
Our evidence suggests that at birth ganglion cells are multiply innervated by preganglionic axons from the brainstem and gland intercalated duct – acinar cell assemblies are multiply innervated by ganglion cells. We assume that the brainstem neurons have different firing patterns at birth (hence presented in blue and red, respectively). The activity patterns of each ganglion cell at birth are thus different because they are each multiply innervated by preganglionic axons that have different synaptic strengths (hence at birth the ganglion cells are each shown in a different color). Analogously, because the gland targets are also multiply innervated, their activity patterns are each different (presented here in different colors). During early postnatal life, these axonal projections begin to be trimmed away. (Left) If synaptic pruning occurred earlier in the ganglion than in the gland (a central to peripheral sequence of maturation) then many ganglion cells would come to have identical activity patterns (by virtue of being singly innervated by the same preganglionic neuron; represented in blue and red, respectively) at a time when their target gland cells are still multiply innervated. Activity dependent competition in the gland could eliminate asynchronous inputs to gland cells (i.e. red and blue inputs to the same target) but could not lead to activity dependent competition between axons driven by the same preganglionic input (i.e. red vs. red or blue vs. blue inputs). This would prevent the emergence of singly innervated gland targets (the gland cells would either have two blue inputs or two red inputs but not only one axon). (Right) However because gland targets are ultimately singly innervated, it seems more likely that the maturation sequence starts in the gland and then progresses centrally. In this alternative, synapse elimination in the gland occurs first, resulting in activity dependent pruning of the inputs of all but one ganglion cell on each gland target. This simplification of circuitry in the gland is then followed by a reorganization and simplification of innervation in the ganglion. This peripheral to central maturation could also extend further upstream into the CNS. Singly innervated ganglion cells and gland cells in the peripheral to central scheme (right) would result in a substantial reduction in axonal branches when compared to the central to peripheral scheme with identical activation precision from the brainstem (left; see text for details).