Coordination, Integration and Behaviour in Invertebrates

Abstract

The production of behaviourally appropriate movements requires coordinating neural interactions within an animal's nervous system, the integration of sensory input from the periphery, and instruction from central neuromodulatory commands. Much of our understanding of the neural correlates of adaptive behaviour has derived from studying the simpler nervous systems of invertebrates.

Keywords: reflexes; rhythmic movement; neural network; motor coordination; sensory feedback

Figure 1.

Coordination of independent muscle effectors. (a) Conjoint contractions of two different muscles (as recorded by electromyography in top left) can be achieved either by electrical coupling (indicated by resistor symbol) between pre‐motor interneurons and/or between motor neurons themselves (not shown). (c) Different muscles can also be coactivated through common innervation from the same motor neuron. (b) Alternate contractions of muscles (see electromyography in top right) can be achieved by reciprocal chemical inhibitory synaptic connections (indicated by stick and ball symbols) between motor neurons (not shown) and/or their pre‐motor interneurons. Relaxation of each muscle occurs passively following its excitation and contraction. (d) Muscle relaxation may be more strictly controlled via additional inhibitory motor innervation that operates coordinately with motor excitation to the antagonistic muscle.

Figure 2.

Synaptic and cellular mechanisms for coordinating rhythmic swimming behaviour in the mollusc Clione. (a) Upstroke and downstroke movements of each wing‐like parapodium are generated by a set of antagonistic pre‐motor interneurons (IN‐u and IN‐d) which excite motor neurons to the corresponding levator and depressor wing muscles. (b) Simultaneous intracellular recordings from such a pair of swim‐generating interneurons showing phase opposition firing, alternating with an inhibitory postsynaptic potential that arises from each impulse in the antagonistic partner. (c) Evidence for post‐inhibitory rebound excitation. An injected hyperpolarizing current pulse (3.5 nA between arrowheads) to mimic synaptic inhibition causes subsequent rebound firing of a swim‐generating interneuron. After Satterlie (1985).

Figure 3.

Schematic representation of motor coordination switching by a single mechanoreceptor neuron in the gastric pattern‐generating network of the lobster. (a) During moderate levels of receptor firing, the higher spontaneous activity of an excitatory (E) sensory interneuron causes it to be preferentially activated, thereby reinforcing the ongoing spontaneous gastric motor rhythm. (b) This output pattern drives contraction of gastric lateral teeth opening (O) in alternate coordination with medial tooth protraction (P). Note that medial tooth protractor and lateral teeth closure (C) motor neurons fire coordinately because of their strong electrical coupling. (c) With higher frequency receptor firing, strong synaptic facilitation in a parallel inhibitory (I) sensory interneuron ensures that this pathway to the gastric circuit now becomes effective, resulting in an immediate reconfiguration of the gastric motor pattern in which the opener and protractor motor neurons now fire coordinate bursts (d). Red‐filled circles in (a) and (c) denote motor neuron subtypes that fire in phase with the mechanoreceptor. After Combes et al. (1999).

Figure 4.

Multiple effects of neuromodulatory neurons on motor network activity and coordination in the lobster stomatogastric nervous system. (a) Electrical stimulation (indicated by hatched bar) of an identified modulatory neuron causes prolonged excitation of the pyloric network: rhythmic bursting in an already active pyloric dilator (PD) neuron is enhanced, while bursting is switched on in a previously silent pyloric (PY) neuron. (b) In contrast, stimulation of another projection neuron (at bar) has the opposite effect; pyloric rhythmicity is drastically slowed, and bursting in the lateral pyloric (LP) neuron is suppressed for several tens of seconds. (c) Functional reconfiguration of the pyloric motor output by cyclic bursting (at bars) in a modulatory input neuron. Note completely different types of motor activity patterns expressed during, immediately following, and several seconds after each discharge in the projection neuron. (d) Modulatory input can dismantle multiple stomatogastric circuits and reconstruct a completely new functional network. When the modulatory neuron is silent, the oesophageal, pyloric and gastric mill networks produce three rhythmic motor patterns that drive separate regional behaviours (basically grinding and food‐filtering movements) in the foregut. After the projection neuron becomes active, these otherwise independent networks are restructured into producing a single conjoint motor pattern, converting the foregut's role from regional food processing to swallowing. (a) After PS Dickinson & F Nagy (1983) Control of a central pattern generator by an identified modulatory interneuron in crustacea. II. Induction and modification of plateau properties in pyloric neurons. Journal of Experimental Biology105: 59–82. (b) After JR Cazalets, F Nagy & M Moulins (1990) Suppressive control of a crustacean pyloric network by a pair of identified interneurons. I. Modulation of a motor pattern. Journal of Neuroscience10: 448–457. (c) After T Bal and F Nagy, unpublished observation. (d) After J Simmers, P Meyrdan, M Moulins (1995) Modulation and dynamic specification of motor rhythm‐generating circuits in crustacea. Journal of Physiology (Paris)89: 195–208.

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Further Reading

Combes D, Meyrand P and Simmers J (1999) Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster. Journal of Neuroscience 19: 3620–3628.

Harris‐Warrick RM and Marder E (1996) Modulation of neural networks for behavior. Annual Review of Neuroscience 14: 39–57.

Hooper SL and Moulins M (1989) Switching of a neuron from one network to another by sensory‐induced changes in membrane properties. Science 244: 1587–1589.

Johnson BR and Harris‐Warrick RM (1990) Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion. Journal of Neuroscience 10: 2066–2076.

Kupfermann I and Weiss KR (1978) The command neuron concept. The Behavioral and Brain Sciences 1: 3–39.

Marder E and Calabrese RL (1996) Principles of rhythmic motor pattern production. Physiological Reviews 76: 687–717.

Nargeot R, Baxter DA and Byrne JH (1999) In vitro analogue of operant conditioning in Aplysia. II. Modifications of the functional dynamics of an identified neuron contribute to motor pattern selection. Journal of Neuroscience 19: 2261–2272.

Nusbaum MP and Beenhakker MP (2002) A small‐systems approach to motor pattern generation. Nature 417: 343–350.

Satterlie R (1985) Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generator. Science 229: 402–404.

Shepherd GM (1994) Neurobiology 3rd edn. New York: Oxford University Press.

Simmers J, Meyrand P and Moulins M (1995) Dynamic networks of neurons. American Scientist 83: 262–268.

Tschuluun N, Hall WM and Mulloney B (2001) Limb movements during locomotion: tests of a model of an intersegmental coordinating circuit. Journal of Neuroscience 21: 7859–7869.

Yu X, Nguyen B and Friesen O (1999) Sensory feedback can co‐ordinate the swimming activity of the leech. Journal of Neuroscience 19: 4634–4643.

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How to Cite close
Combes, Denis, and Simmers, John(May 2005) Coordination, Integration and Behaviour in Invertebrates. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0003639]