Brain Research 887 2000 63–69 www.elsevier.com locate bres
Research report
Polycyclic neuromodulation of the feeding rhythm of the pond snail Lymnaea stagnalis by the intrinsic octopaminergic interneuron, OC
´ Christopher J.H. Elliott , Agnes Vehovszky
Department of Biology , University of York, PO Box 373, York YO10 5YW, UK
Accepted 12 September 2000
Abstract
We have examined the role of the octopamine-containing buccal OC interneuron in the fictive feeding rhythm generated by depolarizing a modulatory interneuron, SO, in the isolated central nervous system CNS of Lymnaea stagnalis. Before stimulating the SO, the initial
fictive feeding rate was 2.060.37 bites min mean6S.E.. When the SO was stimulated, the fictive feeding rate more than doubled, increasing by 5.462.6 bites min. Prestimulation of OC facilitates the ability of the modulatory neuron SO to drive fictive feeding 4 s
later. Following OC stimulation, the increase in SO-driven feeding rate was 10.861.6 bites min, significantly more than when only the SO was stimulated P,0.02, paired t-test on five preparations. OC activity is not required during the SO stimulation for this
enhancement. The maximum of the SO driven rhythm occurs between 6 and 12 s after the end of the OC stimulation at 20 bites min. This is the maximum feeding rate of intact Lymnaea in sucrose. Facilitation is mimicked by bath applied octopamine at 5 mM. Facilitation is
specific to OC interneurons, as the same prestimulation of the electrically coupled neuron N3P central pattern generator interneurons does not affect the feeding rhythm. The OC interneuron acts as a long term, polycyclic modulator, which peaks several feeding cycles
after the OC activity.
2000 Elsevier Science B.V. All rights reserved.
Keywords : Mollusc; Octopamine; Long-term; Polycyclic; Snail; Interneuron
1. Introduction manipulate the cycle in which it is stimulated intra-cyclic
modulation, or it may have effects that last for many A central feature of the organisation of rhythmically
cycles. Such polycyclic modulators are of particular be- active systems is that the pattern generator neurons are
havioural interest because they provide mechanisms to influenced by many modulatory neurons. One way to
translate a transient stimulus into a persisting response and classify neuromodulators is by their function: they may
to allow plasticity of behaviour, for example accelerating trigger the pattern, alter its intensity or rate and even
ingestion once a palatable food has been found. Polycyclic reconfigure its phasing. An example from the feeding
modulation has not been described for any of the protrac- system of the pond snail Lymnaea is the SO interneuron in
tion phase interneurons described in Lymnaea so far; but the buccal ganglia. This can activate fictive feeding in a
the objective of this paper is to show that the swallowing quiescent preparation, accelerate and intensify it if fictive
phase OC interneurons identified recently [21] have a clear feeding is already occurring [16] and produce a change in
polycyclic role. the phase pattern [3]. However, the SO does not participate
Another classification of neuromodulators [9] divides in all the feeding rhythms, for example those driven by
them into extrinsic or intrinsic, with the main criterion N1L or CV1 [14], Fig. 9, [24], Fig. 9.
being that the intrinsic modulators receive rhythmically Neuromodulatory cells may also be separated according
patterned inputs from the pattern generator. On this basis, to the time-scale of their effects: an interneuron may
the SO can be classified as an intrinsic modulator, since it receives weak excitation and strong inhibition from the
central pattern generator circuit, irrespective of whether it is active or not [5]. Other intrinsic modulators of the
Lymnaea feeding system include the protraction phase
Corresponding author. Tel.: 144-190-443-2812; fax: 144-190-443-
interneurons CV1 [14] and CBWC [15] in the cerebral
2860. E-mail address
: cje2york.ac.uk C.J.H. Elliott.
ganglia and the N1L [24] interneurons in the buccal
0006-8993 00 – see front matter
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ganglia. The OC interneurons are also intrinsic neuro- 2. Materials and methods
modulators of the feeding system, because they receive regular inhibitory inputs in the N1 protraction and N2
Pond snails, Lymnaea stagnalis were obtained from rasp phases of the feeding rhythm [21].
dealers Blades Biological, Kent, UK and fed on lettuce. There are just three OC octopamine immunoreactive
The circumoesophageal and buccal ganglia were isolated interneurons in the buccal ganglia [2]. They are weakly
and neurons impaled as described previously [7,21]. The electrically coupled together and do not fire 1:1 action
large buccal motoneurons were visually identified [1] and potentials when one is stimulated. During fictive feeding,
the feeding interneurons, SO, N1L, N3p and OC were they tend to fire in the third, swallowing, phase of the
identified by probing in their usual positions, and checking rhythm. In some preparations the OC cells rarely fire
their identity by firing pattern and interneuronal con- action potentials, but usually their firing rate increases as
nections with the motoneurons [4,5,21,24]. The preparation fictive feeding is driven more strongly, with a maximum
was bathed in normal Lymnaea saline [6]. Octopamine was firing rate in the isolated central nervous system CNS
obtained from Sigma Poole, Dorset, UK. being 15 Hz. They are always robustly inhibited in the first
two phases of the rhythm protraction and rasp and these inputs are always present [20,21].
3. Experimental design
