NEUROSCIENCE An Electrifying Memory

Electric organ discharge (EOD) frequency in the weakly electric brown ghost knife fish (Apteronotus leptorhynchus), which is set by the pacemaker nucleus (PMn, which contains pacemaker and relay neurons), increases in response to a similar frequency EOD or electronic stimulus (which jams the fish's electrosensory system). This jamming avoidance response (JAR) depends on activation of glutamatergic inputs to N-methyl-D-aspartate (NMDA) receptors on the relay neurons. Oestreich et al., who previously described long-term frequency elevation (LTFE), a form of cellular memory in which EOD frequency remains increased for hours after a prolonged jamming stimulus, measured neural correlates of JAR and LTFE in response to afferent stimulation in PMn slices. The magnitude of LTFE depended on the total number of stimuli and not on stimulus frequency or pattern. Further, like LTFE induced by a brief tetanic burst, LTFE in response to prolonged low-frequency stimulation was sensitive to blockade of NMDA receptors. The N-type Ca²⁺ channel blocker -conotoxin GVIA prevented initiation of JAR and LTFE without affecting basal firing frequency, whereas -conotoxin GVIA had no effect on established LTFE. This suggests that LTFE induction--but not its maintenance--depends on synaptic input. NMDA application also elicits LTFE (LTFE_NMDA), and the magnitude of LTFE_NMDA was reduced by decreasing extracellular Ca²⁺ concentration. Stimulus-induced LTFE and LTFE_NMDA were both sensitive to blockade of transient receptor potential (TRP) channels; moreover, TRPM5, which is activated by intracellular Ca²⁺, was cloned from PMn RNA and localized to pacemaker and relay neurons by in situ hybridization. Thus, the authors propose that LTFE occurs in the PMn and that, although it is initiated by synaptic input, its maintenance depends on Ca²⁺-dependent activation of TRP channels and the ensuing neuronal depolarization.

J. Oestreich, N. C. Dembrow, A. A. George, H. H. Zakon, A "sample-and-hold" pulse-counting integrator as a mechanism for graded memory underlying sensorimotor adaptation. Neuron 49, 577-588 (2006). [PubMed]