Repetition Priming of Motoneuronal Activity in a Small Motor Network: Intercellular and Intracellular Signaling

Abstract

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.

Repetition-Induced Plasticity of Motor Representations of Action Sounds

“…Repetition priming of motoneuronal activity has been previously described in the feeding network of aplysia, where repeated stimulation led to an increase in the firing rate of neurons (Friedman et al 2009). The repetition enhancement has been interpreted as an intrinsic characteristic of a network dedicated to motor behavior (Friedman and Weiss 2010). Such an interpretation is, however, unlikely for our results.…”

Feedforward Compensation Mediated by the Central and Peripheral Actions of a Single Neuropeptide Discovered Using Representational Difference Analysis

“…Thus, the peripheral actions of ATRP should be additive. Moreover, because peptides are released more with more activity of the peptide-containing neuron (Whim and Lloyd, 1989; Vilim et al, 1996b, b), and peptide actions tend to be persistent (Fox and Lloyd, 2001; Koh and Weiss, 2005; Friedman and Weiss, 2010), it is likely that peripheral actions of ATRP may buildup as more programs are elicited, thereby providing stronger compensation during the behavior. There may be additional peptides in ATRP-containing neurons, and these peptides could also contribute to feedforward compensation.…”

Functional consequences of neuropeptide and small-molecule co-transmission

“…CBI-2 activates the feeding motor programme in part via its convergent presynaptic facilitation of its cholinergic synaptic actions (FCAP and CP2 act on autoreceptors on CBI-2) and alters the electrophysiological properties of a feeding-related motor neuron 70–72 . In motor neurons B-15 and B-16, the co-released peptides elicit functionally antagonistic actions 21–23 , as one peptide co-transmitter increases muscle contraction amplitude, and the other increases its relaxation rate.…”