Computational mechanisms of mechanosensory processing in the cricket

Abstract

SUMMARY Crickets and many other orthopteran insects face the challenge of gathering sensory information from the environment from a set of multi-modal sensory organs and transforming these stimuli into patterns of neural activity that can encode behaviorally relevant stimuli. The cercal mechanosensory system transduces low frequency air movements near the animal's body and is involved in many behaviors including escape from predators, orientation with respect to gravity, flight steering, aggression and mating behaviors. Three populations of neurons are sensitive to both the direction and dynamics of air currents:an array of mechanoreceptor-coupled sensory neurons, identified local interneurons and identified projection interneurons. The sensory neurons form a functional map of air current direction within the central nervous system that represents the direction of air currents as three-dimensional spatio-temporal activity patterns. These dynamic activity patterns provide excitatory input to interneurons whose sensitivity and spiking output depend on the location of the neuronal arbors within the sensory map and the biophysical and electronic properties of the cell structure. Sets of bilaterally symmetric interneurons can encode the direction of an air current stimulus by their ensemble activity patterns, functioning much like a Cartesian coordinate system. These interneurons are capable of responding to specific dynamic stimuli with precise temporal patterns of action potentials that may encode these stimuli using temporal encoding schemes. Thus, a relatively simple mechanosensory system employs a variety of complex computational mechanisms to provide the animal with relevant information about its environment.

Ca2+ imaging of cricket protocerebrum responses to air current stimulation

“…2). Most cercal ascending interneurons have simple directional tuning curves with a single peak [1,10,19]. Further electrophysilogical experiments using intracellular recording and anatomical studies would reveal the details of the neuronal circuit that achieves complex processing, including direction-specific inhibition, in the VLNP.…”

“…It has been suggested that stimulus direction is not represented topographically in the protocerebrum, unlike in the TAG [12,13,27]. More cells responded to air currents from the front than from behind; however, cercal sensory afferents and ascending interneurons including GIs have low sensitivity to stimuli directly in front of the animal [1,10,18]. As suggested by the reduction of the spike responses in the antennae-removed experiments, these cells could be activated by mechanosensory input from antennae stimulated by air currents.…”

“…In contrast, primary sensory circuits for input provided by thoracic and abdominal sensory organs are located within the lower ganglia. For example, in the cricket, auditory input from the tympanal organ is processed by sound-sensitive interneurons within the prothoracic ganglion [7], and the primary neural circuitry of the cercal sensory system that detects surrounding air currents is located within the terminal abdominal ganglion (TAG) [10].…”

Danger detection and escape behaviour in wood crickets

“…The function of the cerci of crickets and cockroaches, as well as the neural elements carrying and processing mechanosensory information have been extensively studied since the early 70s. Since then the cercal sensory system has become a classical model in neuro-ethology of sensory integration and behavioural guidance (Jacobs et al, 2008;Ritzmann, 1993).…”

“…Studies on these insects focused on the neural basis of wind-detection (Bacon and Murphey, 1984;Jacobs and Miller, 1985;Jacobs andTheunissen, 1996, 2000;Jacobs et al, 1986Jacobs et al, , 2008Miller and Jacobs, 1984;Miller et al, 1991;Murphey, 1981;Paydar et al, 1999;Yono and Shimozawa, 2008), on the escape behaviour (Gras and Hö rner, 1992;Kanou et al, 1999Kanou et al, , 2006Tauber and Camhi, 1995;Schrader, 2000), and on the plasticity and recovery after cercal ablation (Kanou and Kondoh, 2004;Kanou et al, 1999Kanou et al, , 2001Kanou et al, , 2002. To stimulate the cerci, most studies employed air-puffs directed towards them.…”