Regulation of short-term associative memory by calcium-dependent protein kinase

Louis D. Matzel, I. Izja Lederhendler, Daniel L. Alkon

Research output: Contribution to journalArticlepeer-review

50 Scopus citations

Abstract

Neural and behavioral correlates of an associative memory in Hermissenda were examined during induction and/or formation of the memory. Hermissenda received either light (conditioned stimulus or CS) and rotation (unconditioned stimulus or US) paired (i.e., Pavlovian conditioning), light and rotation unpaired (pseudoconditioning), or no exposure to light and rotation. Following 9 pairings in a 6 min session, conditioned animals exhibited a contraction of the foot in response to a test CS presented 2 min after the last conditioning trial, whereas pseudoconditioned and untreated animals exhibited a foot extension to the same CS. In addition, both an associative and a nonassociative reduction in light-induced locomotion was observed. To examine neural correlates of this learning within minutes of acquisition, the isolated nervous system of the Hermissenda (containing the visual and vestibular organs) was trained with stimulus conditions identical to those used for the intact animal. Prior isolation and preparation of the nervous system permitted immediate intracellular recording following the final conditioning trial. Relative to pseudoconditioned and untreated animals, the B photoreceptors in conditioned nervous systems were found to have elevated input resistance (inversely related to K+ channel conductance and positively related to excitability) and exhibited increased steady-state depolarization in response to the light CS, as well as a prolonged depolarization after the CS offset. These neural correlates of the associative memory were attenuated if the protein kinase inhibitor H7 was present in the extracellular bath during conditioning, demonstrating in the reduced preparation that antagonism of protein kinase activity blocks the induction of membrane alterations of identified neurons that correlate with memory storage. In a final experiment, in vitro conditioning was conducted in which discrete light steps were presented paired or unpaired with depolarizing current injected across the B cell soma membrane (to simulate rotation-induced depolarization). A pairing-specific, cumulative depolarization (presumably Ca2+-induced) of the B cell was observed that was accompanied by, and outlasted by, an increase in membrane resistance that persisted for at least 10 min. The increase in resistance (but not the cumulative depolarization) was blocked by H7 and sphingosine, which inhibit the activity and activation, respectively, of protein kinase C (PKC) and calmodulin-dependent protein kinase (CaM kinase). In contrast, HA1004, an inhibitor of the cAMP-dependent protein kinase, did not block the induction of elevated resistance. These results suggest that regulation of ion channel conductance by PKC and/or CaM kinase is an important early stage in the induction of associative memory in Hermissenda.

Original languageEnglish (US)
Pages (from-to)2300-2307
Number of pages8
JournalJournal of Neuroscience
Volume10
Issue number7
DOIs
StatePublished - 1990

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

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