Coordination of Distinct Motor Structures through Remote Axonal Coupling of Projection Interneurons

Abstract

Complex behaviors often require coordinated movements of dissimilar motor structures. The underlying neural mechanisms are poorly understood. We investigated cycle-by-cycle coordination of two dissimilar feeding structures in Aplysia californica: the external lips and the internal radula. During feeding, the lips open while the radula protracts. Lip and radula motoneurons are located in the cerebral and buccal ganglia respectively, and radula motoneurons are controlled by a well-characterized buccal central pattern generator (CPG). Here, we examined whether the three electrically-coupled lip motoneurons C15/16/17 are controlled by the buccal CPG or by a previously-postulated cerebral CPG. Two buccal-cerebral projection interneurons, B34 and B63, which are part of the buccal CPG and mediate radula protraction, monosynaptically excite C15/16/17. Recordings from the B34 axon in the cerebral ganglion demonstrate its direct electrical coupling with C15/16/17, eliminating the need for a cerebral CPG. Moreover, when the multifunctional buccal CPG generates multiple forms of motor programs due to the activation of two inputs: the command-like neuron CBI-2 and the esophageal nerve (EN), C15/16 exhibit activity patterns that are distinct from C17. These distinct activity patterns result from combined activity of B34 and B63 and their differential excitation of C15/16 vs. C17. In more general terms, we identified neuronal mechanisms that allow a single CPG to coordinate the phasing and activity of remotely-located motoneurons innervating distinct structures that participate in the production of different motor outputs. We also demonstrated that axo-dendritic electrical coupling by projection interneurons plays a pivotal role in coordinating activity of these remotely-located neurons.

Functional Organization and Adaptability of a Decision-Making Network in Aplysia

“…In isolated in vitro buccal ganglia preparations, whether spontaneously active or subjected to tonic electrical stimulation of peripheral sensory nerves, this bilateral network continues to generate the motor patterns that underlie the essential features of radula movements and their variability observed in the freely behaving animal (Figures 2A,B; Morton and Chiel, 1993b; Nargeot et al, 1997; Jing et al, 2011). These “fictive” in vitro patterns are therefore composed of successive protraction and retraction phases of changeable durations and in variable overlap with closure motor nerve discharge.…”

“…The interneurons, motor, and sensory neurons responsible for producing and adjusting radula movements are distributed in two interconnected and essentially identical neuronal circuits located within the bilateral buccal ganglia situated on the buccal mass (Kupfermann, 1974 ; Elliott and Susswein, 2002 ). In isolated in vitro buccal ganglia preparations, whether spontaneously active or subjected to tonic electrical stimulation of peripheral sensory nerves, this bilateral network continues to generate the motor patterns that underlie the essential features of radula movements and their variability observed in the freely behaving animal (Figures 2 A,B; Morton and Chiel, 1993b ; Nargeot et al, 1997 ; Jing et al, 2011 ). These “fictive” in vitro patterns are therefore composed of successive protraction and retraction phases of changeable durations and in variable overlap with closure motor nerve discharge.…”

Characterization of GdFFD, a d-Amino Acid-containing Neuropeptide That Functions as an Extrinsic Modulator of the Aplysia Feeding Circuit

“…Electrophysiology-Intracellular and extracellular recordings of the physiological activity from CNS preparations (including the cerebral and buccal ganglia) were performed as described previously (53). The ganglia were desheathed, transferred to a recording chamber containing ϳ1.5 ml of ASW, continuously perfused at 0.3 ml/min, and maintained at 14 -17°C.…”

Different microcircuit responses to comparable input from a one vs. both copies of an identified projection neuron

“…The role(s) of presynaptic regulation of projection-and sensory neuron inputs to microcircuits remains under-explored despite its established presence, often at multiple locations, in several neural systems (Nusbaum, 1994;Sillar and Simmers, 1994;Krieger et al, 1996;Cochilla and Alford, 1999;Westberg et al, 2000;Takahashi and Alford, 2002;Evans et al, 2003;Hurwitz et al, 2005;Barriere et al, 2008;Nusbaum, 2008, 2012;Jing et al, 2011;Wang, 2012;McGann, 2013;Sirois et al, 2013;Blitz et al, 2019). For the MCN1-gastric mill rhythm, the pivotal role of LG neuron presynaptic inhibition of MCN1 STG suggests that this circuit design favors dual MCN1 activity over firing rate-matched single MCN1 activity.…”