Postsynaptic calcium, but not cumulative depolarization, is necessary for the induction of associative plasticity in Hermissenda

Louis D. Matzel, Ronald F. Rogers

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Abstract

The neuronal modifications that underlie associative memory in Hermissenda have their origins in a synaptic interaction between the visual and vestibular systems, and can be mimicked by contiguous in vitro stimulation of these converging pathways. At the offset of vestibular stimulation (i.e., hair cell activity), the B photoreceptors are briefly released from synaptic inhibition resulting in a slight depolarization (2-4 mV). If contiguous pairings of light-induced depolarization and presynaptic vestibular activity occur in close temporal succession, this depolarization "accumulates" and has been hypothesized to culminate in a sustained rise in intracellular Ca2+ and a resultant Ca2+-mediated phosphorylation of K+ channels as well as an associated increase in input resistance. Here we demonstrate that this cumulative depolarization is neither necessary nor sufficient for the biophysical modifications of the B cell membrane indicative of memory formation. Consistent with several recent reports of one-trial learning in Hermissenda, one pairing of light with mechanical stimulation of the vestibular hair cells resulted in a rise in neuronal input resistance across the B cell membrane that was attenuated by a preparing iontophoretic injection of the Ca2+ chelator EGTA (25 mM), indicating that this potentiation was Ca2+ dependent. However, the use of a single pairing negates the possibility of an accumulation of depolarization across trials. In a subsequent experiment, B photoreceptors underwent a cumulative depolarization, and a coincident rise in input resistance, during multiple pairings of light and hair cell stimulation. However, if the B photoreceptor was voltage clamped at its initial resting potential before and after each pairing, thus eliminating the cumulative depolarization, the rise in resistance not only persisted, but was enhanced. Moreover, if unpaired light presentations were followed by a current-induced depolarization (to mimic cumulative depolarization), no increase in input resistance was detected. To assess directly the effect of a cumulative depolarization on the voltage-dependent Ca2+ current, an analysis of the inward current on the B cell soma membrane was conducted. It was determined that (1) the inward current may undergo a partial inactivation during sus-tained depolarization, (2) the peak current was depressed during repetitive depolarizations, and (3) the peak current underwent a steady-state inactivation, such that it was reduced when elicited from holding potentials more positive than -60 mV. The analysis of this current suggests that pairings of light and presynaptic activity would reduce voltage-dependent Ca2+ influx when those pairings are conducted at depolarized membrane potentials, such as during cumulative depolarization. In total, these results indicate that while the cumulative depolarization is a reliable correlate of in vitro conditioning, it does not contribute to the acquisition process per se, while contiguous pre- and postsynaptic activity, and the associated rise in postsynaptic Ca2+, is critical to this process. These results suggest certain similarities to other activity-dependent models of learning-induced plasticity.

Original languageAmerican English
Pages (from-to)5029-5040
Number of pages12
JournalJournal of Neuroscience
Volume13
Issue number12
StatePublished - 1993

ASJC Scopus subject areas

  • General Neuroscience

Keywords

  • Associative learning
  • Barium currents
  • Calcium currents
  • Hermissenda
  • Long-term potentiation
  • Memory
  • Potassium currents

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