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Biomedical subjects

Davide Zoccolan

Publications and source records attributed to Davide Zoccolan.

6 recordsLinked to original sources

Statistics of decision making in the leech.

Animals continuously decide among different behaviors, but, even in invertebrates, the mechanisms underlying choice and decision are unknown. In this article, leech spontaneous behavior was tracked and quantified for up to 12 h. We obtained a statistical characterization, in space and time domains, of the decision processes underlying selection of behavior in the leech. We found that the spatial distribution of leech position in a uniform environment is isotropic (the same in all directions), but this isotropy is broken in the presence of localized external stimuli. In the time domain, transitions among behaviors can be described by a Markov process, the structure of which (allowed states and transitions) is highly conserved across individuals. Finally, a wide range of recurrent, deterministic motifs was identified in the apparently irregular and unstructured exploratory behavior. These results provide a rigorous description of the inner dynamics that control the spontaneous and continuous flow of behavioral decisions in the leech.

Animals↗

Quantitative characterization and classification of leech behavior.

This paper describes an automatic system for the analysis and classification of leech behavior. Three colored beads were attached to the dorsal side of a free moving or pinned leech, and color CCD camera images were taken of the animal. The leech was restrained to moving in a small tank or petri dish, where the water level can be varied. An automatic system based on color processing tracked the colored beads over time, allowing real-time monitoring of the leech motion for several hours. At the end of each experimental session, six time series (2 for each bead) describing the leech body motion were obtained. A statistical analysis based on the speed and frequency content of bead motion indicated the existence of several stereotypical patterns of motion, corresponding to different leech behaviors. The identified patterns corresponded to swimming, pseudo-swimming, crawling, exploratory behavior, stationary states, abrupt movements, and combinations of these behaviors. The automatic characterization of leech behavior demonstrated here represents an important step toward understanding leech behavior and its properties. This method can be used to characterize the behavior of other invertebrates and also for some small vertebrates.

Animals↗

Dynamics and reproducibility of a moderately complex sensory-motor response in the medicinal leech.

Local bending, a motor response caused by mechanical stimulation of the leech skin, has been shown to be remarkably reproducible, in its initial phase, despite the highly variable firing of motoneurons sustaining it. In this work, the reproducibility of local bending was further analyzed by monitoring it over a longer period of time and by using more intact preparations, in which muscle activation in an entire body segment was studied. Our experiments showed that local bending is a moderately complex motor response, composed of a sequence of four different phases, which were consistently identified in all leeches. During each phase, longitudinal and circular muscles in specific areas of the body segment acted synergistically, being co-activated or co-inhibited depending on their position relative to the stimulation site. Onset and duration of the first phase were reproducible across different trials and different animals as a result of the massive co-activation of excitatory motoneurons sustaining it. The other phases were produced by the inhibition of excitatory and activation of inhibitory motoneurons, and also by the intrinsic relaxation dynamics of leech muscles. As a consequence, their duration and relative timing was variable across different preparations, whereas their order of appearance was conserved. These results suggest that, during local bending, the leech neuromuscular system 1) operates a reduction of its available degrees of freedom, by simultaneously recruiting groups of otherwise antagonistic muscles and large populations of motoneurons; and 2) ensures reliability and effectiveness of this escape reflex, by guaranteeing the reproducibility of its crucial initial phase.

Animals↗

Interneurone bursts are spontaneously associated with muscle contractions only during early phases of mouse spinal network development: a study in organotypic cultures.

For a short time during development immature circuits in the spinal cord and other parts of the central nervous system spontaneously generate synchronous patterns of rhythmic activity. In the case of the spinal cord, it is still unclear how strongly synchronized bursts generated by interneurones are associated with motoneurone firing and whether the progressive decline in spontaneous bursting during circuit maturation proceeds in parallel for motoneurone and interneurone networks. We used organotypic cocultures of spinal cord and skeletal muscle in order to investigate the ontogenic evolution of endogenous spinal network activity associated with the generation of coordinate muscle fibre contractions. A combination of multiunit electrophysiological recordings, videomicroscopy and optical flow computation allowed us to measure the correlation between interneurone firing and motoneurone outputs after 1, 2 and 3 weeks of in vitro development. We found that, in spinal organotypic slices, there is a developmental switch of spontaneous activity from stable bursting to random patterns after the first week in culture. Conversely, bursting recorded in the presence of strychnine and bicuculline became increasingly regular with time in vitro. The time course of spontaneous activity maturation in organotypic slices is similar to that previously reported for the spinal cord developing in utero. We also demonstrated that spontaneous bursts of interneurone action potentials strongly correlate with muscular contractions only during the first week in vitro and that this is due to the activation of motoneurones via AMPA-type glutamate receptors. These results indicate the occurrence in vitro of motor network development regulating bursting inputs from interneurones to motoneurones.

Action Potentials↗

Highly variable spike trains underlie reproducible sensorimotor responses in the medicinal leech.

The nervous system of the leech is a particularly suitable model to investigate neural coding of sensorimotor responses because it allows both observation of behavior and the simultaneous measurement of a large fraction of its underlying neuronal activity. In this study, we used a combination of multielectrode recordings, videomicroscopy, and computation of the optical flow to investigate the reproducibility of the motor response caused by local mechanical stimulation of the leech skin. We analyzed variability at different levels of processing: mechanosensory neurons, motoneurons, muscle activation, and behavior. Spike trains in mechanosensory neurons were very reproducible, unlike those in motoneurons. The motor response, however, was reproducible because of two distinct biophysical mechanisms. First, leech muscles contract slowly and therefore are poorly sensitive to the jitter of motoneuron spikes. Second, the motor response results from the coactivation of a population of motoneurons firing in a statistically independent way, which reduces the variability of the population firing. These data show that reproducible spike trains are not required to sustain reproducible behaviors and illustrate how the nervous system can cope with unreliable components to produce reliable action.

Action Potentials↗

Using optical flow to characterize sensory-motor interactions in a segment of the medicinal leech.

Activation of motoneurons innervating leech muscles causes the appearance of a two-dimensional vector field of deformations on the skin surface that can be fully characterized using a new technique (Zoccolan et al., 2001) based on the computation of the optical flow, the two-dimensional vector field describing the point displacements on the skin. These vector fields are characterized by their origin (i.e., the singular point) and by four elementary components that combine linearly: expansion (or compression), rotation, longitudinal shear, and oblique shear. All motoneurons can be classified and recognized according to the components of the deformations they elicit: longitudinal motoneurons give rise almost exclusively to longitudinal negative shear, whereas circular motoneurons give rise to both positive longitudinal shear and significant negative expansion. Oblique motoneurons induce strong oblique shear, in addition to longitudinal shear and negative expansion. Vector fields induced by the contraction of longitudinal, circular, and oblique fibers superimpose linearly. Skin deformations can therefore be attributed rather reliably to the contraction of distinct longitudinal, circular, and oblique muscle fibers. We compared the deformation patterns produced by touching the skin with those produced by intracellular stimulation of P, T, and N cells: vector fields resulting from the activation of P cells were almost identical to those produced by mechanical stimulation. Therefore, motor responses triggered by light or moderate touch are almost entirely mediated by excitation of P cells, with minor contributions from T and N cells.

Action Potentials↗