Chemoreception and mechanoreception in the gastropod molluscPleurobranchaea californica

Abstract

1. Sensory reception in the molluscPleurobranchaea californica was studied in whole animals and surgically reduced preparations by delivering chemical and mechanical stimuli while observing behavior or recording extracellularly the responses of the corresponding nerves. Sensory structures studied included the rhinophores, tentacles and oral veil. 2. Specimens reliably (50% or more) exhibited feeding responses to 10 of 18 amino acids tested (Table 1), including alanine and glycine. In 14 electrophysiological experiments on the rhinophore, medium to high centripetal responses to alanine and/or glycine were obtained in 7 preparations (Fig. 2), while little or no response was obtained in 7 preparations. Responses to different amino acids were sometimes mediated by the same centripetal unit (Fig. 2). 3. The rhinophore nerves showed vigorous excitatory responses to variations in the salt concentration (Figs. 3, 4), osmolarity (Figs. 5, 6), and pH (Figs. 7, 8) of sea water solutions directed onto the rhinophore sensory epithelium. The rhinophore and tentacle nerves showed strong excitatory responses to various salt solutions directed onto the corresponding sensory structure, including 1 osmolar NaCl, NaBr, NaI, Na2SO4 and KCl, but not LiCl (Table 2). Curves relating extracellular discharge to stimulus strength typically showed a minimum in the physiological range and increases to either side of this range (Figs. 4, 8). 4. All nerves studied showed excitatory responses to stimulation with mechanical stimuli (Figs. 9–11). Maps of receptive fields of different nerves (Fig. 10) delineated areas of functional innervation for each nerve and showed little overlap. The same centripetal unit(s) typically responded to mechanostimulation of a wide peripheral area (Fig. 11). 5. All nerves studied showed excitatory responses to application of liquefied food substances to the sensory structures (Figs. 12–15). Dose response curves for different food stimuli (Fig. 13) were similar except at higher stimulus strengths, where mean discharge rates were significantly different for different foods. These and other data furnish neurophysiological evidence for discrimination between different food stimuli, as suggested also by earlier behavioral studies (Davis et al. 1980). 6. For all stimuli, severing the afferent nerves leading from the peripheral sensory epithelium abolished electrophysiological responses. Therefore the responses observed were mediated by the sensory epithelium rather than by direct stimulation of peripheral ganglia or nerves. 7. It is concluded that the rhinophores, tentacles and oral veil participate not only in food detection but also have the sensory capacity to detect changes in several other environmental parameters. The data are consistent with the hypothesis that incoming afferent information is processed by peripheral ganglia before it is relayed centrally.