Sacral preganglionic neurons are essential to the neural control of the excretory and sex organs. Previously employed multi-cell tracing methods have certain limitations in the precise morphological analysis of the neural pathways that control these organs. These limitations were overcome by the intracellular injection of neurobiotin or horseradish peroxidase into single preganglionic neurons in the lateral sacral parasympathetic nucleus of the cat. Following light microscopic examination, these neurons, as a group, were found to have an average of five stem dendrites, which divided into 15 dendritic end-branches that were distributed among eight dendritic terminal fields. These dendrites had a major transverse orientation and were quite long, many of them reaching well into the dorsal and ventral horns and into the dorsal gray commissure. These dendrites also exhibited a major longitudinal orientation, extending an average of 869 microns (combined length of rostral and caudal dendrites) within the nucleus. Two groups of cells emerged on the basis of different dendritic patterns. Cells classed as Type I had dendrites in lamina I and in the ventral horn but lacked a significant projection into the lateral funiculus. Cells classed as Type II had major dendritic projections into the lateral funiculus but lacked dendrites in lamina I. The diverse dendritic patterns of these two cell types indicate dissimilar afferent control mechanisms and suggest that these preganglionic neurons may innervate different target organs.

The classic view of preganglionic neurons in spinal autonomic nuclei is that they convey information exclusively from the central nervous system to autonomic neurons in peripheral ganglia. The present morphological study in the cat sacral spinal cord demonstrates that these neurons may also make abundant synaptic connections within the spinal cord.Neurons labeled intracellularly with neurobiotin or horseradish peroxidase exhibited an expansive distribution of axon collaterals in spinal cord laminae I, V, VII, Vm, IX, X, and the ventrolateral funiculi. This broad-ranging axon-collateral system, which has the potential for multiple neuronal contacts, indicates widespread integrative functions for sacral preganglionic neurons within the spinal cord, in addition to functions currently known in the periphery.The preganglionic neuron of the autonomic nervous system represents the first component of a two-neuron efferent pathway that carries information from the central nervous system to the visceral organs. These neurons, which are located in the spinal cord-many of them in the intermediolateral cell column-and in visceral motor nuclei in the brainstem, integrate afferent inputs from various central and peripheral sources and then convey efferent signals to ganglion cells in the peripheral nervous system.According to traditional concepts, preganglionic neurons have purely peripheral functions and do not make efferent connections with other neurons in the central nervous system. However, in the sacral parasympathetic preganglionic pathways to the urinary bladder of the cat, a bilateral and intersegmental recurrent inhibitory mechanism has been identified using electrophysiological techniques (1-3). These findings raise the possibility that sacral preganglionic neurons have an axon-collateral system that makes synaptic contacts with inhibitory interneurons within the spinal cord similar to axon-collateral pathways that have been identified for somatic motoneurons (4). Numerous morphological studies have failed to confirm the existence of sacral preganglionic axon collaterals (5-9). However, in the present experiments extensive axon-collateral systems have been revealed by using intracellular labeling techniques. MATERIALS AND METHODSIn these experiments, 20 male cats were anesthetized with diallylbarbituric acid (0.3 mg/kg) and urethane (2.4 mg/kg i.p.) supplemented with sodium pentobarbital (30 mg/kg i.v.), as needed. After a laminectomy, neurons in the sacral spinal cord were activated antidromically by electrical stimulation of the S2 ventral root and identified as preganglionic neurons by having stimulus thresholds two to three times higher than those of motoneurons and by their slow conduction velocities of 4-12 m/sec. These neurons were located in lateral lamina VII in an area of the sacral parasympathetic nucleus known to contain bladder preganglionic neurons (6, 8) and had conduction velocities typical of these cells (1, 10). Electrodes were judged to be intracellular when resting membrane potentials dro...