title: Encoding of Tactile Stimuli by Mechanoreceptors and Interneurons of the Medicinal Leech.
abstract: For many animals processing of tactile information is a crucial task in behavioral contexts like exploration, foraging, and stimulus avoidance. The leech, having infrequent access to food, developed an energy efficient reaction to tactile stimuli, avoiding unnecessary muscle movements: The local bend behavior moves only a small part of the body wall away from an object touching the skin, while the rest of the animal remains stationary. Amazingly, the precision of this localized behavioral response is similar to the spatial discrimination threshold of the human fingertip, although the leech skin is innervated by an order of magnitude fewer mechanoreceptors and each midbody ganglion contains only 400 individually identified neurons in total. Prior studies suggested that this behavior is controlled by a three-layered feed-forward network, consisting of four mechanoreceptors (P cells), approximately 20 interneurons and 10 individually characterized motor neurons, all of which encode tactile stimulus location by overlapping, symmetrical tuning curves. Additionally, encoding of mechanical force was attributed to three types of mechanoreceptors reacting to distinct intensity ranges: T cells for touch, P cells for pressure, and N cells for strong, noxious skin stimulation. In this study, we provide evidences that tactile stimulus encoding in the leech is more complex than previously thought. Combined electrophysiological, anatomical, and voltage sensitive dye approaches indicate that P and T cells both play a major role in tactile information processing resulting in local bending. Our results indicate that tactile encoding neither relies on distinct force intensity ranges of different cell types, nor location encoding is restricted to spike count tuning. Instead, we propose that P and T cells form a mixed type population, which simultaneously employs temporal response features and spike counts for multiplexed encoding of touch location and force intensity. This hypothesis is supported by our finding that previously identified local bend interneurons receive input from both P and T cells. Some of these interneurons seem to integrate mechanoreceptor inputs, while others appear to use temporal response cues, presumably acting as coincidence detectors. Further voltage sensitive dye studies can test these hypotheses how a tiny nervous system performs highly precise stimulus processing.
authors.affiliation: Computational Neuroscience, Department of Neuroscience, University of OldenburgOldenburg, Germany; Cluster of Excellence Hearing4all, University of OldenburgOldenburg, Germany.
authors.forename: Jutta
authors.initials: J
authors.lastname: Kretzberg
authors.affiliation: Computational Neuroscience, Department of Neuroscience, University of OldenburgOldenburg, Germany; Department of Organismal Biology and Anatomy, University of ChicagoChicago, IL, USA.
authors.forename: Friederice
authors.initials: F
authors.lastname: Pirschel
authors.affiliation: Computational Neuroscience, Department of Neuroscience, University of Oldenburg Oldenburg, Germany.
authors.forename: Elham
authors.initials: E
authors.lastname: Fathiazar
authors.affiliation: Computational Neuroscience, Department of Neuroscience, University of OldenburgOldenburg, Germany; Faculty of Medical Sciences, Institute of Neuroscience, Newcastle UniversityNewcastle upon Tyne, UK.
authors.forename: Gerrit
authors.initials: G
authors.lastname: Hilgen
keywords: hirudo; local bend; mechanoreception; pressure; skin stimulation; somatosensory system; touch; voltage sensitive dye