Multiple types of control by identified interneurons in a sensory-activated rhythmic motor pattern.

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Kemenes, György ; Staras, Kevin ; Benjamin, Paul R (2001)

Modulatory interneurons that can drive central pattern generators (CPGs) are considered as good candidates for decision-making 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.
  • References (60)
    60 references, page 1 of 6

    Arshavsky YI, Deliagina TG, Meizerov ES, Orlovsky GN, Panchin YV (1988a) Control of feeding movements in the freshwater snail Planorbis corneus. I. Rhythmical neurons of buccal ganglia. E xp Brain Res 70:310 -322.

    Arshavsky YI, Deliagina TG, Orlovsky GN, Panchin YV (1988b) Control of feeding movements in the freshwater snail Planorbis corneus. III. Organization of the feeding rhythm generator. E xp Brain Res 70:332-341.

    Arshavsky YI, Deliagina TG, Orlovsky GN, Panchin YV (1989) Control of feeding movements in pteropod mollusc Clione limacina. E xp Brain Res 78:387-397.

    Benjamin PR (1983) Gastropod feeding: behavioral and neural analysis of a complex multicomponent system. In: Neural origin of rhythmic movements (Roberts A, Roberts B, eds). C ambridge, UK : C ambridge UP.

    Benjamin PR, Elliott C JH (1989) Snail feeding oscillator: The central pattern generator and its control by modulatory interneurons. In: Neuronal and cellular oscillators (Jacklet J, ed), pp 173-214. New York: Dekker.

    Benjamin PR, Winlow W (1981) The distribution of three wide-acting synaptic inputs to identified neurons in the isolated brain of Lymnaea. Comp Biochem Physiol [A] 70:293-307.

    Benjamin PR, Staras K , Kemenes G (2000) A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn Mem 7:124 -131.

    Blitz DM, Nusbaum M P (1999) Distinct f unctions for cotransmitters mediating motor pattern selection. J Neurosci 19:6774 - 6783.

    Brierley MJ, Yeoman MS, Benjamin PR (1997) Glutamatergic N2v cells are central pattern generator interneurons of the Lymnaea feeding system: a new model for rhythm generation. J Neurophysiol 78:3396 -3407.

    Bu¨schges A, Manira AE (1998) Sensory pathways and their modulation in the control of locomotion. Curr Opin Neurobiol 8:733-739.

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