Neuronal competition for action potential initiation sites in a circuit controlling simple learning

Neuroscience. 2007 Aug 10;148(1):65-81. doi: 10.1016/j.neuroscience.2007.05.046. Epub 2007 Jul 17.

Abstract

The spatial and temporal patterns of action potential initiations were studied in a behaving leech preparation to determine the basis of increased firing that accompanies sensitization, a form of non-associative learning requiring the S-interneurons. Little is known at the network level about mechanisms of behavioral sensitization. The S-interneurons, one in each ganglion and linked by electrical synapses with both neighbors to form a chain, are interposed between sensory and motor neurons. In sensitized preparations the strength of shortening is related to S-cell firing, which itself is the result of impulses initiating in several S-cells. Because the S-cells, as independent initiation sites, all contribute to activity in the chain, it was hypothesized that during sensitization, increased multi-site activity increased the chain's firing rate. However, it was found that during sensitization, the single site with the largest initiation rate, the S-cell in the stimulated segment, suppressed initiations in adjacent ganglia. Experiments showed this was both because (1) it received the earliest, greatest input and (2) the delayed synaptic input to the adjacent S-cells coincided with the action potential refractory period. A compartmental model of the S-cell and its inputs showed that a simple, intrinsic mechanism of inexcitability after each action potential may account for suppression of impulse initiations. Thus, a non-synaptic competition between neurons alters synaptic integration in the chain. In one mode, inputs to different sites sum independently, whereas in another, synaptic input to a single site precisely specifies the overall pattern of activity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Electric Stimulation
  • Electrical Synapses / physiology
  • Ganglia, Invertebrate / cytology
  • Ganglia, Invertebrate / physiology
  • Hirudo medicinalis / cytology
  • Hirudo medicinalis / physiology*
  • Interneurons / cytology
  • Interneurons / physiology*
  • Learning / physiology*
  • Nerve Net / cytology
  • Nerve Net / physiology
  • Nervous System Physiological Phenomena*
  • Neural Pathways / cytology
  • Neural Pathways / physiology*
  • Neurons, Afferent / physiology
  • Reflex / physiology
  • Refractory Period, Electrophysiological / physiology
  • Synaptic Transmission / physiology