The Tactile Receptive Fields of Freely Moving Caenorhabditis elegans Nematodes

Abstract

Sensory neurons embedded in skin are responsible for the sense of touch. In humans and other mammals, touch sensation depends on thousands of diverse somatosensory neurons. By contrast, Caenorhabditis elegans nematodes have six gentle touch receptor neurons linked to simple behaviors. The classical touch assay uses an eyebrow hair to stimulate freely moving C. elegans, evoking evasive behavioral responses.While this assay has led to the discovery of genes required for touch sensation, it does not provide control over stimulus strength or position. Here, we present an integrated system for performing automated, quantitative touch assays that circumvents these limitations and incorporates automated measurements of behavioral responses. Highly Automated Worm Kicker (HAWK) unites microfabricated silicon force sensors and video analysis with real-time force and position control. Using this system, we stimulated animals along the anterior-posterior axis and compared responses in wild-type and spc-1(dn) transgenic animals, which have a touch defect due to expression of a dominant-negative a spectrin protein fragment.As expected from prior studies, delivering large stimuli anterior to the mid-point of the body evoked a reversal, but such a stimulus applied posterior to the mid-point evoked a speed-up. The probability of evoking a response of either kind depended on stimulus strength and location; once initiated, the magnitude and quality of both reversal and speed-up behavioral responses were uncorrelated with stimulus location, strength, or the absence or presence of the spc-1(dn) transgene. Wild-type animals failed to respond when the stimulus was applied near the mid-point. These results establish that stimulus strength and location govern the activation of a stereotyped motor program and that the C. elegans body surface consists of two receptive fields separated by a gap.

Tissue mechanics and somatosensory neural responses govern touch sensation inC. elegans

“…A second alternative exploits the architecture of C. elegans neurons: TRNs extend longitudinally for about half of the nematode’s length, leaving a region around its center that is relatively insensitive to touch (see [43]). Fig.…”

“…9C and G, with the noise levels better controlled and the stimulation point moved along the longitudinal axis so as to assay a variable number of channels. The ideal experiment would be to precisely assay the neural response to stimuli in the central dead-zone of the body, where few channels are likely to be directly stimulated (see [43]).…”

Temporal processing and context dependency in Caenorhabditis elegans response to mechanosensation

“…The six soft-touch mechanosensory neurons detect both spatially localized and non-localized stimuli. Anterior touches are detected by anterior neurons ALML, ALMR and AVM and evoke reversal behaviors whereas posterior touches are detected by posterior neurons PLML and PLMR and evoke forward sprints ( Chalfie and Sulston, 1981 ; Chalfie et al, 1985 ; McClanahan et al, 2017 ; Mazzochette et al, 2018 ). Non-spatially localized plate taps are detected by both anterior and posterior soft-touch neurons and evoke reversals in young adult animals ( Chalfie and Sulston, 1981 ; Rankin et al, 1990 ); on rare occasions, they also evoke forward acceleration ( Wicks and Rankin, 1995 ; Chiba and Rankin, 1990 ).…”

“…The animal’s behavior response to mechanosensory stimuli has primarily been studied using impulse stimuli. Specifically, the stimuli were either a brief application of touch, tap or optogenetic stimulation, and the most salient feature of these stimuli was their amplitude, not their temporal profile ( Petzold et al, 2013 ; Stirman et al, 2011 ; McClanahan et al, 2017 ; Mazzochette et al, 2018 ). In the classical touch assay, for example, a saturating force that lasts just a few tenths of a second is applied ( Nekimken et al, 2017 ).…”

“…Over short timescales, reversals or accelerations depend on the set of neurons stimulated and the stimulus strength. The location of an applied force determines which touch receptor neurons are activated and thus whether the animal accelerates or reverses, while the amplitude of the applied stimulus determines the probability that the animal responds at all ( Driscoll, 1997 ; Stirman et al, 2011 ; Petzold et al, 2013 ; McClanahan et al, 2017 ; Mazzochette et al, 2018 ).…”