Abstract
The tiny ensemble of neurons in the leech ganglion can discriminate the locations of touch stimuli on the skin as precisely as a human fingertip. The leech uses this ability to locally bend the body-wall away from the stimulus. It is assumed that a three-layered feedforward network of pressure mechanoreceptors, interneurons, and motor neurons controls this behavior. Most previous studies identified and characterized the local bend network based on electrical stimulation of a single pressure mechanoreceptor, which was sufficient to trigger the local bend response. Recent studies showed, however, that up to six mechanoreceptors of three types innervating the stimulated patch of skin carry information about both touch intensity and location simultaneously. Therefore, we hypothesized that interneurons involved in the local bend network might require the temporally concerted inputs from the population of mechanoreceptors representing tactile stimuli, to decode the tactile information and to provide appropriate synaptic inputs to the motor neurons. We examined the influence of current injection into a single mechanoreceptor on activity of postsynaptic interneurons in the network and compared it to responses of interneurons to skin stimulation with different pressure intensities. We used voltage-sensitive dye imaging to monitor the graded membrane potential changes of all visible cells on the ventral side of the ganglion. Our results showed that stimulation of a single mechanoreceptor activates several local bend interneurons, consistent with previous intracellular studies. Tactile skin stimulation, however, evoked a more pronounced, longer-lasting, stimulus intensity-dependent network dynamics involving more interneurons. We concluded that the underlying local bend network enables a non-linear processing of tactile information provided by population of mechanoreceptors. This task requires a more complex network structure than previously assumed, probably containing polysynaptic interneuron connections and feedback loops. This small, experimentally well-accessible neuronal system highlights the general importance of selecting adequate sensory stimulation to investigate the network dynamics in the context of natural behavior.
Highlights
Understanding the mechanisms of how sensory information is conveyed onto motor neurons to elicit behavioral reactions is a major goal in neuroscience
We study the activity of the local bend network driven either by electrical stimulation of a single pressure mechanoreceptor or by natural tactile stimulation on the skin involving the activation of 4–6 mechanoreceptors
We recorded the response of an AP cell intracellularly while imaging the whole ganglion with voltage-sensitive dye (VSD) in a body-wall preparation
Summary
Understanding the mechanisms of how sensory information is conveyed onto motor neurons to elicit behavioral reactions is a major goal in neuroscience. One or several layers of interneurons connect the sensory receptors to motor neurons. Depending on the behavioral context, these interneurons provide synaptic inputs to motor neurons, generating different motor patterns in the same, or overlapping, sets of muscles (Pearson, 1993; Büschges et al, 2011). The leech nervous system is a useful model to understand the role of interneurons in tactile processing (Wagenaar, 2015). A small sensory-motor network in the leech elicits surprisingly precise behavioral patterns. Leeches produce different motor patterns when locally bending away from stimulus locations that are only separated by 1 mm on their body-wall (Baca, 2005; Kristan et al, 2005)
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