The differences in the anatomy of the thoracolumbar and sacral autonomic outflow are quantitative

Abstract

Purpose: We have re-evaluated the anatomical arguments that underlie the division of the spinal visceral outflow into sympathetic and parasympathetic divisions.

Methodology: Using a systematic literature search, we mapped the location of catecholaminergic neurons throughout the mammalian peripheral nervous system. Subsequently, a narrative method was employed to characterize segment-dependent differences in the location of preganglionic cell bodies and the composition of white and gray rami communicantes.

Results and conclusion: One hundred seventy studies were included in the systematic review, providing information on 389 anatomical structures. Catecholaminergic nerve fibers are present in most spinal and all cranial nerves and ganglia, including those that are known for their parasympathetic function. Along the entire spinal autonomic outflow pathways, proximal and distal catecholaminergic cell bodies are common in the head, thoracic, and abdominal and pelvic region, which invalidates the "short-versus-long preganglionic neuron" argument. Contrary to the classically confined outflow levels T1-L2 and S2-S4, preganglionic neurons have been found in the resulting lumbar gap. Preganglionic cell bodies that are located in the intermediolateral zone of the thoracolumbar spinal cord gradually nest more ventrally within the ventral motor nuclei at the lumbar and sacral levels, and their fibers bypass the white ramus communicans and sympathetic trunk to emerge directly from the spinal roots. Bypassing the sympathetic trunk, therefore, is not exclusive for the sacral outflow. We conclude that the autonomic outflow displays a conserved architecture along the entire spinal axis, and that the perceived differences in the anatomy of the autonomic thoracolumbar and sacral outflow are quantitative.

Keywords: Autonomic nervous system; Ganglion; Neural crest cells; Neuron; Postganglionic; Preganglionic.

Fig. 1

Definitive catecholaminergic cell positions. References are plotted showing the position of cell bodies along the cranio-caudal (Y) and proximo-distal (X) body axes. Altogether, the data show that both proximal and distal ganglia are common in the entire thoracolumbar and sacral autonomic outflow pathways. Other references indicate the levels at which preganglionic neurons bypass the sympathetic trunk (curved arrows), or more frequently use the gray rami communicantes (brown stars)

Fig. 2

Catecholaminergic neurons in the human geniculate ganglion and the greater superficial petrosal nerve. Example of a TH-positive cell body (A) and nerve fiber (B) in the geniculate ganglion and proximal course of the superficial petrosal nerve, respectively. Nerve tissue was harvested from a formalin-fixed cadaver (97 years of age) from the body donation program of the Department of Anatomy and Embryology, Maastricht University. The body was preserved by intra-arterial infusion with 10 L fixative (composition (v/v): 21% ethanol, 21% glycerin, 2% formaldehyde, 56% water, and 16 mmol/L thymol), followed by 4 weeks of fixation in 20% ethanol, 2% formaldehyde, and 78% water. Antibody: Abcam ab209487, 1:10,000. Antigen retrieval Tris–EDTA pH 9.0, 30 min. Secondary antibody GAR-bio, 1:10,000. Chromogen: Vector NovaRED peroxidase substrate kit, SK-4805

Fig. 3

Cranio-caudal change in the position of the cell bodies and the course of the preganglionic neurons. Simplified representation. Left: Preganglionic outflow at the levels T1-L2 and S2-S4. The “lumbar gap” is indicated by an asterisk. Dashed outflow: preganglionic neurons within the “lumbar gap.” Right: From the lower margin of the thoracolumbar outflow downward (panel 1), a gradually increasing number (represented by arrow thickness) of preganglionic neurons originate from cell bodies within or near the ventral motor nuclei and bypass the sympathetic trunk (panels 2 and 3, neuron Y). Bypassing the sympathetic trunk, therefore, is not exclusive for the sacral outflow. Lumbar splanchnic nerves can arise directly from the lumbar plexus (Panel 2, f), such as pelvic splanchnic nerves arise from the sacral plexus (Panel 3, f′). Panels 1 and 2, neuron X: Classic representation of a preganglionic neuron with its cell body in the intermediolateral nucleus. Labels are identical in all panels; a: sympathetic trunk ganglion, b: spinal nerve, c: spinal ganglion, d: rami communicantes, e: splanchnic nerves

Fig. 4

Scheme of neurons using two or more nerves to reach their target organ. Neuronal function is not strictly coupled to specific nerves: neurons change course (purple) from nerve A to nerve B and C via communicating nerve branches (asterisks). This behavior could fit a still hypothetical peripheral connectome