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When a behavior is repeated performance often improves, i.e., repetition priming occurs. Although repetition priming is ubiquitous, mediating mechanisms are poorly understood. We address this issue in the feeding network ofAplysia Similar to the priming observed elsewhere, priming inAplysiais stimulus specific, i.e., it can be either "ingestive" or "egestive." Previous studies demonstrated that priming alters motor and premotor activity. Here we sought to determine whether sensorimotor transmission is also modified. We report that changes in sensorimotor transmission do occur. We ask how they are mediated and obtain data that strongly suggest a presynaptic mechanism that involves changes in the "background" intracellular Ca(2+)concentration ([Ca(2+)]i) in primary afferents themselves. This form of plasticity has previously been described and generated interest due to its potentially graded nature. Manipulations that alter the magnitude of the [Ca(2+)]iimpact the efficacy of synaptic transmission. It is, however, unclear how graded control is exerted under physiologically relevant conditions. In the feeding system changes in the background [Ca(2+)]iare mediated by the induction of a nifedipine-sensitive current. We demonstrate that the extent to which this current is induced is altered by peptides (i.e., increased by a peptide released during the repetition priming of ingestive activity and decreased by a peptide released during the repetition priming of egestive activity). We suggest that this constitutes a behaviorally relevant mechanism for the graded control of synaptic transmission via the regulation of the [Ca(2+)]iin a neuron., (Copyright © 2016 the American Physiological Society.)

Two distinct mechanisms mediate potentiating effects of depolarization on synaptic transmission. Recently there has been renewed interest in a type of plasticity in which a neuron's somatic membrane potential influences synaptic transmission. We study mechanisms that mediate this type of control at a synapse between a mechanoafferent, B21, and B8, a motor neuron that receives chemical synaptic input. Previously we demonstrated that the somatic membrane potential determines spike propagation within B21. Namely, B21 must be centrally depolarized if spikes are to propagate to an output process. We now demonstrate that this will occur with central depolarizations that are only a few millivolts. Depolarizations of this magnitude are not, however, sufficient to induce synaptic transmission to B8. B21-induced postsynaptic potentials (PSPs) are only observed if B21 is centrally depolarized by >or=10 mV. Larger depolarizations have a second impact on B21. They induce graded changes in the baseline intracellular calcium concentration that are virtually essential for the induction of chemical synaptic transmission. During motor programs, subthreshold depolarizations that increase calcium concentrations are observed during one of the two antagonistic phases of rhythmic activity. Chemical synaptic transmission from B21 to B8 is, therefore, likely to occur in a phase-dependent manner. Other neurons that receive mechanoafferent input are electrically coupled to B21. Differential control of spike propagation and chemical synaptic transmission may, therefore, represent a mechanism that permits selective control of afferent transmission to different types of neurons contacted by B21. Afferent transmission to neurons receiving chemical synaptic input will be phase specific, whereas transmission to electrically coupled followers will be phase independent.

Although central pattern generators (CPGs) can produce rhythmic activity in isolation, it is now generally accepted that under physiological conditions information from the external and internal environment is incorporated into CPG-induced motor programs. Experimentally advantageous invertebrate preparations may be particularly useful for studies that seek to characterize the cellular mechanisms that make this possible. In these experiments, we study sensorimotor integration in the feeding circuitry of the mollusc Aplysia. We show that a premotor neuron with plateau properties, B51, is important for generating the radula closing/retraction phase of ingestive motor programs. When B51 is depolarized in semi-intact preparations, radula closing/retractions are enhanced. When B51 is hyperpolarized, radula closing/retractions are reduced in size. In addition to being important as a premotor interneuron, B51 is also a sensory neuron that is activated when the feeding apparatus, the radula, rotates backward. The number of centripetal spikes in B51 is increased if the resistance to backward rotation is increased. Thus, B51 is a proprioceptor that is likely to be part of a feedback loop that insures that food will be moved into the buccal cavity when difficulty is encountered. Our data suggest, therefore, that Aplysia are able to adjust feeding motor programs to accommodate the specific qualities of the food ingested because at least one of the neurons that generates the basic ingestive motor program also serves as an on-line monitor of the success of radula movements.

1. The accessory radula closer (ARC) muscle of Aplysia californica and its innervation is a model preparation for the study of the neural and cellular mechanisms of behavioral plasticity. Much of the plasticity is mediated by release of neurotransmitters and peptide cotransmitters that modulate contractions of the muscle. Preliminary to investigating the cellular mechanisms of action of these modulators, we have characterized the major membrane ion currents present in the unmodulated ARC muscle and their likely roles in normal contraction. We have studied single dissociated but functionally intact ARC muscle fibers under voltage clamp. This is the second of three papers describing this work. In the preceding paper we described the electrophysiological properties of the fibers at hyperpolarized voltages, and characterized the two major hyperpolarized-activated currents present, a classical inwardly rectifying K current and a Cl current induced by elevated intracellular Cl-. 2. In this paper we dissect the large outward current that becomes activated when the fibers are depolarized above -50 or -40 mV. We find that this current consists of two major depolarization-activated K currents, a fast transient "A"-type current and a slower maintained delayed rectifier, with perhaps a small component of Ca(2+)-activated K current. 3. The A current begins to activate with voltage steps above -50 or -40 mV. It activates in milliseconds, then inactivates virtually completely within 100-200 ms. It is fully available for activation below -80 mV, and almost completely inactivated above -40 mV. It is Ca2+ independent, half-maximally blocked by approximately 3 mM 4-aminopyridine (4-AP) but only 460 mM tetraethylammonium (TEA). 4. The delayed rectifier both activates and inactivates more slowly and more positive than the A current. Thus it begins to activate only above -30 or -20 mV; it activates in tens of milliseconds, then inactivates incompletely over several seconds; it is fully available below -70 mV and inactivated above 0 mV. It is Ca2+ independent, half-maximally blocked by 10 mM TEA and 3-10 mM 4-AP. 5. In the following paper we describe a depolarization-activated Ca current that underlies the K currents and most likely provides Ca2+ necessary for contraction of the muscle. By activating simultaneously with the Ca current, the K currents serve to prevent spikes, so that the depolarization is confined to a range where small voltage changes provide fine control over a wide range of contraction strengths.

1. The accessory radula closer (ARC) muscle of Aplysia californica and its innervation is a model preparation for the study of the neural and cellular mechanisms of behavioral plasticity. Much of the plasticity is due to modulation of contractions of the muscle by a variety of neurotransmitters and peptide cotransmitters. Preliminary to investigating the cellular mechanisms of this modulation, we have characterized the major membrane ion currents present in the unmodulated ARC muscle and their likely roles in normal contraction. We have studied single dissociated but functionally intact ARC muscle fibers under voltage clamp. This is the last of three papers describing this work. In the first paper we characterized two currents prominent at hyperpolarized voltages, a classical inwardly rectifying K current and a Cl current induced by elevated intracellular Cl-. In the second paper we examined two large outward K currents activated at more depolarized voltages, an "A" current and a delayed rectifier. 2. In this paper, we describe an inward depolarization-activated Ca current that underlies and is normally completely masked by the K currents and is revealed when they are blocked. 3. The Ca current begins to activate above -40 or -30 mV. It is fully available for activation at voltages more negative than -60 mV. It activates in milliseconds, then inactivates relatively slowly with maintained depolarization. The current is larger and inactivates slower when it is carried by Ba2+ rather than Ca2+. The inactivation is current rather than voltage dependent. The current is blocked by Co2+, Cd2+, and with a characteristic time dependence, by the dihydropyridine Ca-channel antagonist nifedipine. 4. These properties of the current characterize it as a high-threshold, L-type Ca current. 5. This current most likely provides Ca2+ necessary for contraction of the ARC muscle.