Neural Circuits: Functional Reconfiguration

Abstract

Animals produce a vast array of behaviours. In part, this ability arises because the neural networks that produce behaviour are multifunctional entities capable of producing many different outputs, and because many different functional neural networks can be created from a single large neuronal assembly.

Keywords: modulation; crustacean stomatogastric system; tritonia; respiration; neuronal switching

Figure 1.

The Tritonia swimming network (a) can exist in two functional configurations, one of which produces withdrawal (b), the other of which produces defensive swimming (c). Closed circles represent inhibitory synapses; bars represent excitatory synapses; combined circles and bars represent synapses that induce, with different time courses, both inhibition and excitation. DSI, Dorsal Swim Interneuron; VSI, Ventral Swim Interneuron; I, Inhibitory interneuron.

Figure 2.

The mouse respiratory rhythm generator can produce in vitro two output patterns, one of which corresponds to the neural activity observed in the intact animal during normal breathing (a), the other to the activity observed in the intact animal during gasping (b). The trace marked XII is an integrated record of extracellular activity on nerve XII; the shaded rectangle marks inspiration. Note the change in pre‐Bötzinger complex (PBC) neuron phase relative to the inspiration.

Figure 3.

Full understanding of the mechanisms underlying network reconfiguration requires consideration of neurons not directly affected by the treatment that induced the reconfiguration. (a) In the intact network proctolin drives the pyloric network of the crustacean stomatogastric system to cycle at 1 Hz, but when the network's pacemaker neuron is isolated from the network, proctolin makes it cycle at almost 2 Hz. (b) Experiments in which the two Pyloric Dilator (PD) neurons were sequentially removed from the network revealed that these neurons, which are not themselves affected by proctolin, are primarily responsible for slowing Anterior Burster (AB) neuron cycling.

Figure 4.

Neuron switching. (a) In the crab several neurons are spontaneously, in a preparation‐specific manner, members of either the pyloric or gastric mill networks. The bars show the percentage of preparations in which the marked neurons functioned with each network (e.g. the Anterior Medial (AM) neuron functioned with each in 50% of preparations). The italicized names indicate that in other decapod crustacea the neuron is exclusively a gastric mill network neuron; the names in roman text indicate that in other species the neuron is exclusively a pyloric network neuron. LG, Lateral Gastric; MG, Median Gastric; Int1, interneuron 1; PY, Pyloric; AB, Anterior Burster; LP, Lateral Pyloric; PD, Pyloric Dilator; VD, Ventricular Dilator; IC, Inferior Cardiac; GM, Gastric Mill. (b) In animals in which the gastric mill network is spontaneously silent, activation of the gastric mill network can induce the Lateral Posterior Gastric (LPG) neuron to cease firing with the pyloric network (monitored by an extracellular recording of the pyloric dilator nerve, pdn) to instead firing with the gastric mill network (monitored by an intracellular recording from the Dorsal Gastric (DG) neuron).

Figure 5.

Network fusion. (a) Application of red pigment concentrating hormone (RPCH) fuses the gastric mill network (monitored by the Lateral Posterior Gastric (LPG) neuron) and the cardiac sac networks (monitored by the Cardiac Dilator (CD) 2 neuron). (b) Stimulation of a descending input can fuse the pyloric network (monitored by the intracellular recording of the Pyloric Dilator (PD) neuron) and the gastric mill network (monitored by the intracellular recordings of the Gastric Mill (GM) and LPG neurons). In both panels, rectangles represent one cycle period of the relevant rhythms.

Figure 6.

Changes in both cellular and synaptic properties can underlie neuron switching and network fusion. (a) Stimulation of a descending input that switches the Ventricular Dilator (VD) neuron from the pyloric to the cardiac sac network also abolishes the ability of the VD neuron to produce plateau potentials. (b) Red pigment concentrating hormone (RPCH), which fuses the gastric mill and cardiac sac networks, dramatically increases the amplitude of cardiac sac synaptic input on to various gastric mill network neurons. The dots represent stimulation of the Inferior Ventricular neurons of the cardiac sac network; note the increased excitatory postsynaptic potential (EPSP) in the Lateral Posterior Gastric (LPG) neuron and the increased inhibitory postsynaptic potential (IPSP) in the Gastric Mill (GM) neuron.

Figure 7.

A changing modulatory milieu can confound investigation of network capabilities at different developmental stages. (a) In the lobster embryo the gastric mill and pyloric networks always produce a single, fused output under control conditions. (b) This fusion does not arise because the two networks do not, at this stage, have the ability to function independently: when descending inputs are blocked, the two networks function independently. In both (a) and (b) an excitatory modulator, oxotremorine, was applied to increase network activity. PD, Pyloric Dilator; DG, Dorsal Gastric.

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References

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Further Reading

Blitz DM and Nusbaum MP (1997) Motor pattern selection via inhibition of parallel pathways. Journal of Neuroscience 17: 4965–4975.

Getting PA (1989) Emerging principles governing the operations of neural networks. Annual Review of Neuroscience 12: 185–204.

Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brooks VB (ed.) Handbook of Physiology, sect. 1, The Nervous System, vol. 2, Motor Control, pp. 1179–1236. Bethesda, MD: American Physiological Society.

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Harris‐Warrick RM, Marder E, Selverston AI and Moulins M (1992) Dynamic Biological Networks: The Stomatogastric Nervous System. Cambridge, MA: MIT Press.

Heinzel HG, Weimann JM and Marder E (1993) The behavioral repertoire of the gastric mill in the crab, Cancer pagurus: an in situ endoscopic and electrophysiological examination. Journal of Neuroscience 13: 1793–1803.

Katz PS and Harris‐Warrick RM (1990) Actions of identified neuromodulatory neurons in a simple motor system. Trends in Neuroscience 13: 367–373.

Marder E, Abbott LF, Buchholtz F et al. (1993) Physiological insights from cellular and network models of the stomatogastric nervous systems of lobsters and crabs. American Zoologist 33: 29–39.

Norris BJ, Coleman MJ and Nusbaum MP (1994) Recruitment of a projection neuron determines gastric mill motor pattern selection in the stomatogastric nervous system of the crab, Cancer borealis. Journal of Neurophysiology 72: 1451–1463.

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Hooper, Scott L(Apr 2001) Neural Circuits: Functional Reconfiguration. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0000114]