Encoding and Decoding Touch Location in the Leech CNS

Thomson, Eric E.; Kristan, William B.

doi:10.1523/jneurosci.5472-05.2006

Cited by 33 publications

(57 citation statements)

References 34 publications

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“…Our computational experiments confirm that temporal information is primarily caused by latency differences between the responses to different stimuli. These results support the importance of response latency as a fundamental element of the neural code (Amassian, 1953;Jones 1956;Gawne et al, 1996;Eggermont, 1998;Raiguel et al, 1999;Oram et al, 2002;Hurley and Pollak, 2005;Thomson and Kristan, 2006;Gollisch and Meister, 2008;Foffani et al, 2008).…”

Section: Informational Contribution Of First-spike Latencies and Jitterssupporting

confidence: 79%

Spike Timing, Spike Count, and Temporal Information for the Discrimination of Tactile Stimuli in the Rat Ventrobasal Complex

Foffani

Morales-Botello²,

Aguilar³

2009

J. Neurosci.

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The aim of this work was to investigate the role of spike timing for the discrimination of tactile stimuli in the thalamic ventrobasal complex of the rat. We applied information-theoretic measures and computational experiments on neurophysiological data to test the ability of single-neuron responses to discriminate stimulus location and stimulus dynamics using either spike count (40 ms bin size) or spike timing (1 ms bin size). Our main finding is not only that spike timing provides additional information over spike count alone, but specifically that the temporal aspects of the code can be more informative than spike count in the rat ventrobasal complex. Virtually all temporal information-i.e., information exclusively related to when the spikes occur-is conveyed by first spikes, arising mostly from latency differences between the responses to different stimuli. Although the imprecision of first spikes (i.e., the jitter) is highly detrimental for the information conveyed by latency differences, jitter differences can contribute to temporal information, but only if latency differences are close to zero. We conclude that temporal information conveyed by spike timing can be higher than spike count information for the discrimination of somatosensory stimuli in the rat ventrobasal complex.

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Section: Informational Contribution Of First-spike Latencies and Jitterssupporting

confidence: 79%

Spike Timing, Spike Count, and Temporal Information for the Discrimination of Tactile Stimuli in the Rat Ventrobasal Complex

Foffani

Morales-Botello²,

Aguilar³

2009

J. Neurosci.

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“…A simple neuronal system produces a basic behavior with a surprisingly high precision: The leech bends away locally from a light touch (Stuart, 1970; Kristan, 1982; Lockery and Sejnowski, 1992; Lewis and Kristan, 1998a; Zoccolan et al, 2002; Baca et al, 2005; Thomson and Kristan, 2006) with a spatial precision of approximately 1 mm (Baca et al, 2005); similar to that of the human fingertip (Johnson, 2001). The different leech mechanoreceptor types show similar spiking patterns to primate and human mechanoreceptor types (Lewis and Kristan, 1998b; Baca et al, 2005; Johansson and Flanagan, 2009; Smith and Lewin, 2009), and mechanoreceptor responses were shown to depend on common stimulus properties like touch location, mechanical force, duration, and speed (leech: Carlton and McVean, 1995; Zoccolan et al, 2002; Baca et al, 2005; Pirschel and Kretzberg, 2016; primate reviews: Johansson and Flanagan, 2009; Abraira and Ginty, 2013; Saal and Bensmaia, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…In all mechanoreceptors the inhomogeneous distribution of dendritic branches and nerve endings in the skin (Blackshaw, 1981; Blackshaw et al, 1982) cause spatially structured receptive fields. Stimulation close to the most densely innervated receptive field center triggers highest spike counts and shortest spike latencies (Nicholls and Baylor, 1968; Thomson and Kristan, 2006; Pirschel and Kretzberg, 2016). …”

Section: Introductionmentioning

confidence: 99%

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Encoding of Tactile Stimuli by Mechanoreceptors and Interneurons of the Medicinal Leech

et al. 2016

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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.

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“…These somatosensory systems rely on interneurons to multiplex and decode signals from multiple classes of sensory neurons. The decoded signal ultimately governs the behavioral response scope; leech responses span global body movements to localized bending 55,56 . This model aligns with our proposed signaling model in which a set of interneurons is responsible for decoding the sensory neuron signal and triggering the behavioral response.…”

Section: Trn-specific Disruption Of Spectrin Network Impairs Touch Smentioning

confidence: 99%

The Tactile Receptive Fields of Freely Moving Caenorhabditis elegans Nematodes

Mazzochette¹,

Nekimken

Loizeau

et al. 2018

Preprint

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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.

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Encoding and Decoding Touch Location in the Leech CNS

Cited by 33 publications

References 34 publications

Spike Timing, Spike Count, and Temporal Information for the Discrimination of Tactile Stimuli in the Rat Ventrobasal Complex

Spike Timing, Spike Count, and Temporal Information for the Discrimination of Tactile Stimuli in the Rat Ventrobasal Complex

Encoding of Tactile Stimuli by Mechanoreceptors and Interneurons of the Medicinal Leech

The Tactile Receptive Fields of Freely Moving Caenorhabditis elegans Nematodes

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