Dual Sensory-Motor Function for a Molluskan Statocyst Network

Abstract

Levi, R., P. Varona, Y. I. Arshavsky, M. I. Rabinovich, and A. I. Selverston. Dual sensory-motor function for a molluskan statocyst network. J Neurophysiol 91: 336 -345, 2004. First published September 24, 2003 10.1152/jn.00753.2003. In mollusks, statocyst receptor cells (SRCs) interact with each other forming a neural network; their activity is determined by both the animal's orientation in the gravitational field and multimodal inputs. These two facts suggest that the function of the statocysts is not limited to sensing the animal's orientation. We studied the role of the statocysts in the organization of search motion during hunting behavior in the marine mollusk, Clione limacina. When hunting, Clione swims along a complex trajectory including numerous twists and turns confined within a definite space. Search-like behavior could be evoked pharmacologically by physostigmine; application of physostigmine to the isolated CNS produced "fictive search behavior" monitored by recordings from wing and tail nerves. Both in behavioral and in vitro experiments, we found that the statocysts are necessary for search behavior. The motor program typical of searching could not be produced after removing the statocysts. Simultaneous recordings from single SRCs and motor nerves showed that there was a correlation between the SRCs activity and search episodes. This correlation occurred even though the preparation was fixed and, therefore the sensory stimulus was constant. The excitation of individual SRCs could in some cases precede the beginning of search episodes. A biologically based model showed that, theoretically, the hunting search motor program could be generated by the statocyst receptor network due to its intrinsic dynamics. The results presented support for the idea that the statocysts are actively involved in the production of the motor program underlying search movements during hunting behavior.

The Role of Sensory Network Dynamics in Generating a Motor Program

“…Despite the consistency of the response, the exact timing of the activity was variable enough between bursts that the relative timing between units could change completely. In previous work (Levi et al, 2004), we showed that the timing of the activation does not change arbitrarily. Rather, the peak activity of each unit was separated from the others, and in many episodes, the sequential order of the activity was preserved.…”

“…Preparations for electrophysiological experiments were made in ice-cold seawater to prevent excitation of nociceptive afferent fibers. The preparation, including cerebral, pedal, and abdominal ganglia with the tail and wing nerves, was pinned to a Sylgard-lined Petri dish as described previously (Levi et al, 2004). Extracellular recordings from nerves were made by using glass suction electrodes or stainless-steel electrodes.…”

“…Fictive hunting behavior was induced by application of physostigmine as in the work by Arshavsky et al (1993) and Levi et al (2004). To achieve fictive hunting, the seawater covering the isolated nervous system was replaced by seawater containing 10 Ϫ6 M physostigmine.…”

“…Previous work has shown that the statocysts are necessary for the production of hunting behavior and that the motor output produces dynamics that are consistent with output generated by a winnerless competition model of the statocyst (Varona et al, 2002;Levi et al, 2004). However, because we were unable to record or manipulate more than one statocyst receptor cell (SRC) at a time, it remained unclear how the output of a population of SRCs corresponds to the actual motor output during hunting.…”

“…Another way to reveal the dynamical properties of the nervous system is by looking at extreme examples of animal behavior. We have suggested previously that statocysts in the mollusk Clione also have the capability of independently generating a motor program (Levi et al, 2004).…”