Abstract
Compared to other neurons of the central nervous system, autonomic preganglionic neurons are unusual because most of their axon lies in the periphery. These axons are vulnerable to injury during surgical procedures, yet in comparison to peripheral neurons and somatic motor neurons, the impact of injury on preganglionic neurons is poorly understood. Here, we have investigated the impact of axotomy on sacral preganglionic neurons, a functionally diverse group of neurons required for micturition, defecation, and sexual function. We have previously observed that after axotomy, the injury-related transcription factor activating transcription factor-3 (ATF3) is upregulated in only half of these neurons (Peddie and Keast, 2011: PMID: 21283532). In the current study, we have investigated if this response is constrained to particular subclasses of preganglionic neurons that have specific functions or signaling properties. Seven days after unilateral pelvic nerve transection, we quantified sacral preganglionic neurons expressing ATF3, many but not all of which co-expressed c-Jun. This response was independent of soma size. Subclasses of sacral preganglionic neurons expressed combinations of somatostatin, calbindin, and neurokinin-1 receptor, each of which showed a similar response to injury. We also found that in contrast to thoracolumbar preganglionic neurons, the heat shock protein-25 (Hsp25) was not detected in naive sacral preganglionic neurons but was upregulated in many of these neurons after axotomy; the majority of these Hsp25 neurons expressed ATF3. Together, these studies reveal the molecular complexity of sacral preganglionic neurons and their responses to injury. The simultaneous upregulation of Hsp25 and ATF3 may indicate a distinct mechanism of regenerative capacity after injury.
Highlights
Autonomic preganglionic neurons are the first relay in peripheral visceral motor pathways
We examined the impact of axotomy on L6-S1 intermediolateral nucleus (IML) populations visualized by FG and each of these markers (SOM, CAL, and neurokinin 1 receptor (NK1R)) (Figure 3)
No effect of the axotomy was evident by visual inspection of the pattern of immunolabeled sections, but the diversity of structures labeled by each antibody and the differences in axonal patterning between IML sections could obscure an effect on the preganglionic neuronal population
Summary
Autonomic preganglionic neurons are the first relay in peripheral visceral motor pathways They are central nervous system (CNS) neurons with a soma located in either spinal cord or brainstem, but like somatomotor neurons are unusual in that most of the axon projects outside of the CNS. These long axons project through peripheral nerves to autonomic postganglionic neurons, making them vulnerable to physical damage. Parasympathetic regulation of urogenital organs and the lower bowel is provided by sacral preganglionic neurons found in the intermediolateral nucleus (IML) below the lumbar spinal cord enlargement By convention, they are identified as sacral preganglionic neurons, but in rodents are found in L6 and S1 spinal cord segments (Hancock and Peveto, 1979). After exiting the spinal cord, sacral preganglionic axons travel together in the pelvic nerves (rodents) or pelvic splanchnic nerves (humans), which is consistent with the profound impact on many pelvic organ functions caused by damage to these nerves, as seen in conus medullaris and cauda equina syndromes (Orendacova et al, 2001; Hoang and Havton, 2006; Hoang et al, 2006)
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