Field effects trigger post-anodal rebound excitation in vertebrate CNS

Abstract

Although both chemical and electrotonic synaptic interactions have often been implicated in normal and pathophysiological conditions where clusters of central neurones discharge in unison^1–5, in many instances the mechanisms underlying synchrony in the vertebrate central nervous system remain obscure. Another form of cellular communication which can be invoked is that of field effects³, defined here as electrical interactions mediated across extracellular space. Studies of the goldfish Mauthner (M-) cell provided the first clear evidence for such interactions, which have now been shown to exist in various mammalian central structures^6–10. A single impulse in the M-cell leads to the nearly simultaneous firing of 40 to 80 inter-neurones which feed inhibition back onto it^11,12, by both direct synaptic excitation and a field effect, which is initially hyper-polarizing. On the basis of early observations on this system, it was suggested that field effects could induce or facilitate synchronized and even epileptic-like neuronal bursting¹³. We report here that the inhibitory interneurones exhibit a remarkably sensitive anodal break excitation triggered by a brief hyperpolarization comparable to the electrical inhibition mentioned above. This mechanism alone may be sufficient to recruit a second class of these interneurones^14,15 , which are postsynaptic to eighth nerve afferents and do not receive chemical synaptic input from the collateral network. The rebound facilitation is distinguished from excitatory field effects which can also contribute to synchronization.