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...