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The Journal of Neuroscience, April 12, 2006, 26(15):4026-4035; doi:10.1523/JNEUROSCI.4727-05.2006

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Behavioral/Systems/Cognitive
Persistent Responses to Brief Stimuli: Feedback Excitation among Brainstem Neurons

Wen-Chang Li,¹ Stephen R. Soffe,¹ Ervin Wolf,² and Alan Roberts¹

¹School of Biological Sciences, University of Bristol, Bristol BS8 1UG, United Kingdom, and ²Department of Anatomy, Medical and Health Science Center, University of Debrecen, Debrecen, Hungary

Correspondence should be addressed to Alan Roberts, School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, United Kingdom. Email: a.roberts{at}bristol.ac.uk

The ability of brief stimuli to trigger prolonged neuronal activity is a fundamental requirement in nervous systems, common to motor responses and short-term memory. Bistable membrane properties and network feedback excitation have both been proposed as suitable mechanisms to sustain such persistent responses. There is now good experimental evidence for membrane bistability. In contrast, the long-standing hypotheses based on positive feedback excitation have yet to be supported by direct evidence for mutual excitatory connections between appropriate neurons. In young frog tadpoles (Xenopus), we show that a small region of caudal hindbrain and rostral spinal cord is sufficient to generate prolonged swimming in response to a brief stimulus. We used paired whole-cell patch recordings to identify hindbrain neurons in this region that actively excite spinal neurons to drive sustained swimming. We show directly that some of these hindbrain neurons make reciprocal excitatory connections with each other. We use a population model of the hindbrain network to illustrate how feedback excitation can provide a robust mechanism to generate persistent responses. Our recordings provide direct evidence for feedback excitation among neurons within a network that drives a prolonged response. Its presence in a lower brain region early in development suggests that it is a basic feature of neuronal network design.

Key words: feedback; locomotion; reticulospinal; rhythm generation; synapses; Xenopus

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Received Nov. 4, 2005; revised Feb. 22, 2006; accepted Feb. 25, 2006.

Correspondence should be addressed to Alan Roberts, School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, United Kingdom. Email: a.roberts{at}bristol.ac.uk

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