Specificity of mono- and divalent salt transduction mechanisms in frog gustation evidenced by cobalt chloride treatment

Abstract

1. Discrimination among stimuli with similar physical properties represents a formidable problem in sensory neurophysiology. The differential effect of cobalt chloride treatment on gustatory responses to monovalent and divalent salts may help to explain aspects of how the frog gustatory system encodes these stimuli. 2. Gustatory neural responses recorded from the glossopharyngeal nerve to divalent stimuli (CaCl2 and MgCl2) were inhibited by CoCl2 treatment, whereas monovalent responses (NaCl and KCl) were greatly augmented. Both effects were highly significant and completely reversible. 3. Intracellular recordings from the gustatory receptor cells, which synaptically initiate the impulses in the glossopharyngeal afferents, imply that these neural events are not a simple reflection of the receptor potential magnitude. Monovalent receptor potentials magnitudes (millivolts of depolarization) were enhanced by cobalt chloride, but receptor potentials to divalent stimuli were not inhibited. Rather they were either unaffected (MgCl2) or augmented (CaCl2). 4. Membrane resistance change during salt stimulation with cobalt chloride treatment followed the qualitative pattern observed with the neural response. Membrane resistance (in megohms) of the receptor cell was greater for divalent stimuli with cobalt treatment compared with divalent stimuli alone. Membrane resistance changes for monovalent stimuli were less with cobalt treatment compared with monovalent stimuli alone. These observations indicate that the glossopharyngeal neural response is not a simple reflection of the magnitude of the receptor potential but must be considered in conjunction with membrane resistance as an indicator of synaptic transmission. 5. These data were interpreted in terms of leading models of salt taste transduction, i.e., adsorption theories, phase boundary theories, and the direct penetration theories. Relevant mechanistic considerations for salt taste transduction in the frog include binding by divalents to membrane surface changes and amiloride-sensitive monovalent cation channels. It was concluded that the surface potential alone was not a critical variable in the mechanism of cobalt chloride alteration of salt responses.