Repetition priming of motoneuronal activity in a small motor network: intercellular and intracellular signaling.

The characteristics of central pattern generator (CPG) outputs are subject to extensive modulation. Previous studies of neuromodulation largely focused on immediate actions of neuromodulators, i.e., actions that were exerted at the time when either neuromodulators were present or neuromodulatory inputs to the CPG were active. However, neuromodulatory actions are known to persist when neuromodulators are no longer present. In Aplysia, stimulation of cerebral-buccal interneuron-2 (CBI-2), which activates the feeding CPG, produces a repetition priming of motor programs. This priming is reflected in an increase of firing of motoneurons. As CBI-2 contains two neuromodulatory peptides, FCAP (feeding circuit-activating peptide) and CP2 (cerebral peptide 2), we hypothesized that repetition priming may involve persistent peptidergic neuromodulation. We find that these peptides produce priming-like effects, i.e., they increase the firing of radula-opening (B48) and radula-closing (B8) motoneurons during motor programs. Proekt et al. (2004, 2007) showed that repetition priming of neuron B8 is implemented by modulatory inputs that B8 receives from the CPG. In contrast, our current findings indicate that priming of B48 may be implemented by a direct peptidergic modulation of its intrinsic characteristics via a pathway that activates cAMP. We suggest that the direct versus indirect, i.e., CPG-dependent, repetition priming may be related to the type of input that individual motoneurons receive from the CPG. We suggest that in motoneurons that are driven by concurrent excitation-inhibition, repetition priming is indirect as it is preferentially implemented via modulation of the output of CPGs. In contrast, in motoneurons that are driven by alternating excitation-inhibition, direct modulation of motoneurons may be preferentially used.