Multiple Types of Control by Identified Interneurons in a Sensory-Activated Rhythmic Motor Pattern

Abstract

Modulatory interneurons that can drive central pattern generators (CPGs) are considered as good candidates for decisionmaking roles in rhythmic behaviors. Although the mechanisms by which such neurons activate their target CPGs are known in detail in many systems, their role in the sensory activation of CPG-driven behaviors is poorly understood. In the feeding system of the mollusc Lymnaea, one of the best-studied rhythmical networks, intracellular stimulation of either of two types of neuron, the cerebral ventral 1a (CV1a) and the slow oscillator (SO) cells, leads to robust CPG-driven fictive feeding patterns, suggesting that they might make an important contribution to natural food-activated behavior. In this paper we investigated this contribution using a lip-CNS preparation in which feeding was elicited with a natural chemostimulant rather than intracellular stimulation. We found that despite their CPG-driving capabilities, neither CV1a nor SO were involved in the initial activation of sucrose-evoked fictive feeding, whereas a CPG interneuron, N1M, was active first in almost all preparations. Instead, the two interneurons play important and distinct roles in determining the characteristics of the rhythmic motor output; CV1a by modulating motoneuron burst duration and SO by setting the frequency of the ongoing rhythm. This is an example of a distributed system in which (1) interneurons that drive similar motor patterns when activated artificially contribute differently to the shaping of the motor output when it is evoked by the relevant sensory input, and (2) a CPG rather than a modulatory interneuron type plays the most critical role in initiation of sensory-evoked rhythmic activity.

Cerebral CBm1 Neuron Contributes to Synaptic Modulation Appearing During Rejection of Seaweed inAplysia kurodai

“…The processing neural network has also been well studied for odor preference (Gelperin and Tank 1990;Gelperin et al 1993;Schütt and Basar 1994). In contrast, the neuronal basis of taste preference has been little studied except for the neural pathway for the chemosensory inputs of the primary food (Bicker et al 1982;Delaney and Gelperin 1990;Kemenes et al 1986Kemenes et al , 2001Rosen et al 1991).…”

Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis

“…Second, the CSOs likely contain both chemosensory and mechanosensory PSCs (de Vlieger, 1968;Jager, 1971;Goldschmeding and Jager, 1973;Janse, 1976;Lever, 1977;Kemenes et al, 1986), thus providing a variety of sensory cell types to be identified. Moreover, examinations of feeding control in L. stagnalis have explored both mechanosensation and chemosensation mediated by the CSOs (Elphick et al, 1995;Staras et al, 1999;Kemenes et al, 2001), adding physiological relevance to our work. Finally, the thin and flat CSOs (Fig.…”

Associative Memory Stored by Functional Novel Pathway rather than Modifications of Preexisting Neuronal Pathways

“…5). This model is built on our detailed knowledge of the feeding circuitry, which includes the cerebralbuccal interneurons (CBIs) (Kemenes et al, 2001;Straub et al, 2004). These are a group of command neurons located in the cerebral ganglia that project to the buccal ganglia, in which they can activate the feeding central pattern generator (Fig.…”

“…Although the CS has been reported to be neutral with respect to feeding Audesirk et al, 1982), we show here that, before conditioning, amyl acetate can both excite and inhibit feeding behavior depending on its concentration. Our knowledge of the Lymnaea feeding system (Benjamin and Elliott, 1989;Benjamin et al, 2000;Kemenes et al, 2001;Straub et al, 2002) allowed us to identify the neural pathways serving the excitatory and inhibitory effects on feeding in naive animals. Their effects on feeding, however, are unaltered by associative conditioning.…”