Positive feedback loops sustain repeating bursts in neuronal circuits

Abstract

Voluntary movements in animals are often episodic, with abrupt onset and termination. Elevated neuronal excitation is required to drive the neuronal circuits underlying such movements; however, the mechanisms that sustain this increased excitation are largely unknown. In the medicinal leech, an identified cascade of excitation has been traced from mechanosensory neurons to the swim oscillator circuit. Although this cascade explains the initiation of excitatory drive (and hence swim initiation), it cannot account for the prolonged excitation (10-100 s) that underlies swim episodes. We present results of physiological and theoretical investigations into the mechanisms that maintain swimming activity in the leech. Although intrasegmental mechanisms can prolong stimulus-evoked excitation for more than one second, maintained excitation and sustained swimming activity requires chains of several ganglia. Experimental and modeling studies suggest that mutually excitatory intersegmental interactions can drive bouts of swimming activity in leeches. Our model neuronal circuits, which incorporated mutually excitatory neurons whose activity was limited by impulse adaptation, also replicated the following major experimental findings: (1) swimming can be initiated and terminated by a single neuron, (2) swim duration decreases with experimental reduction in nerve cord length, and (3) swim duration decreases as the interval between swim episodes is reduced.

Specialized brain regions and sensory inputs that control locomotion in leeches

“…It was previously reported that removal of the tail ganglion shortens swim duration in preparations with the head brain removed (Brodfuehrer et al 1993; Puhl and Mesce 2010; Friesen et al 2011). We were interested in determining whether the presence of the tail ganglion was necessary for the occurrence of the extended swims in preparations with only the SupraEG removed.…”

“…Because cell 204 is a crucial component of the swim maintenance system (Weeks and Kristan 1978; Friesen et al 2011), cycle period can be considered a good measure of the excitation level in this system. We used this relationship to ask whether, in addition to extending swim duration, the maintenance system in SubEG-T preparations also has higher activity levels.…”

“…Interestingly, the presence of prolonged swims in SubEG-T preparations requires the presence of the tail brain. It is already known that the removal of tail brain shortens swim duration in preparations with or without the head brain attached (Brodfuehrer et al 1993; Friesen et al 2011). However, here, removing the tail brain not only shortened, but completely eliminated the extended swims observed in SubEG-T preparations.…”

A classic model animal in the 21st century: recent lessons from the leech nervous system

“…In a further modeling effort synthesizing a career-spanning series of experimental studies, Friesen et al (2011) constructed a network model comprising multi-compartmental neurons of the entire swimming circuit, including trigger and gating neurons not shown in Fig. 2B.…”

Detection of noise effect on coupled neuronal circuits

“…On the other hand, neuronal activities of neurons have also been investigated by using PSpice tool or artificial neuronal circuit [41][42][43][44][45][46][47]. In the case for circuit implementation, the integrated circuits [51,52] are often used for building amplifiers or experimental circuit elements, while some researcher prefer to using commercial amplifiers as well because of its availabity and easy accessibility.…”