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The sacral autonomic outflow is sympathetic

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Science  18 Nov 2016:
Vol. 354, Issue 6314, pp. 893-897
DOI: 10.1126/science.aah5454

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  • RE: “The sacral autonomic outflow is sympathetic” (Science, 18th November, p. 893)
    • John P. Horn, Professor of Neurobiology, University of Pittsburgh, School of Medicine, Pittsburgh, PA
    • Other Contributors:
      • William C. de Groat, Distinguished Professor of Pharmacology and Chemical Biology, Department of Pharmacology and Chemical Biology, Department of Pharmacology and Chemical Biology

    Functional criteria define divisions of the autonomic motor system

    In a recent report, Espinosa-Medina et al.(1) conclude that ‘The sacral autonomic (i.e. parasympathetic) outflow is sympathetic’. We disagree. Langley(2) and other pioneers defined the sympathetic, parasympathetic and enteric autonomic divisions by observing functional responses to nerve stimulation, lesions and drugs. Understanding the system’s developmental origins came much later, beginning with experiments using deletions and chimeras(3). By focusing on embryos at one developmental stage (E13.5), Espinosa-Medina et al. have drawn attention to transcription factors that may guide the early lineage of preganglionic and ganglionic neurons at different levels of the neuroaxis. Although intriguing, these findings lack quantitation and do not explain the organization of neuronal phenotypes within ganglia or of spinal microcircuits that drive different behaviors. Each division of the autonomic system contains ganglia with multiple neuronal phenotypes that are defined by target specificity (e.g. vasoconstrictor, pilomotor, detrusor motor). For example, thermoregulatory behaviors coordinate piloerection, cutaneous vasoconstriction, and activation of brown fat through the paravertebral sympathetic ganglia, while sexual behavior requires integration of sacral parasympathetic outflow with thoracic sympathetic outflow. In addition, the present results fail to explain why the sacral autonomic outflow d...

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    Competing Interests: None declared.
  • RE: “The sacral autonomic outflow is sympathetic” (Science, 18th November, p. 893)
    • Wilfrid Jänig, Emeritus Professor, Physiologisches Institut, Christian-Albrechts-Universität zu Kiel, Germany
    • Other Contributors:
      • Janet Keast, Professor and Head, Department of Anatomy and Neuroscience, University of Melbourne, Melbourne, Australia
      • Elspeth McLachlan, Emeritus Professor and Visiting Senior Principal Research Fellow, University of New South Wales and Neuroscience Research Australia
      • Winfried Neuhuber, Professor and Head, Insitut für Anatomie, Universität Erlangen-Nürnberg, Erlangen, Germany
      • Michelle Southard-Smith, Associate Professor of Medicine and Cell & Developmental Biology, Vanderbilt University Medical Center, Nashville, USA

    With their provocative title, “The sacral autonomic outflow is sympathetic” (1, 18th November, p. 893), Espinosa-Medina et al. propose that the sacral spinal outflow be reclassified, because some aspects have more in common with thoracolumbar (i.e. sympathetic) than cranial (i.e. parasympathetic) circuits during fetal development. They misquote some anomalies of function and over-emphasise rare deviations observed in adult mammals. These fail to support abolishing the current schema. Acceptance of this reckless distortion of the sympathetic and parasympathetic systems (2) risks prejudicing rather than enhancing translational research and clinical practice.

    Some of the “evidence” presented is not novel or surprising. Cranial nuclei develop in a distinct environment and differentiate earlier than the sacral cord and the pelvic innervation. The work ignores anterior-posterior temporal maturation of the nervous system that impacts on the timing of gene expression patterns (3-5). Their conclusions are based on a selective and in some cases only transient phenotype at E13.5.

    Key functional (often antagonistic) differences between sympathetic and parasympathetic pathways to the pelvic organs have been well described (6,7). These include parasympathetic increases in motility of bladder and hindgut and erection of penis but sympathetically-mediated relaxation. Sympathetic but no parasympathetic pathways constrict most blood vessels, sphincters and the internal repro...

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    Competing Interests: None declared.