Synaptic transmission of graded membrane potential changes and spikes between identified visual interneurons

Abstract

Several physiological mechanisms allow sensory information to be propagated in neuronal networks. According to the conventional view of signal processing, graded changes of membrane potential at the dendrite are converted into a sequence of spikes. However, in many sensory receptors and several types of mostly invertebrate neurons, graded potential changes have a direct impact on the cells' output signals. The visual system of the blowfly Calliphora vicina is a good model system to study synaptic transmission in vivo during sensory stimulation. We recorded extracellularly from an identified motion-sensitive neuron while simultaneously measuring and controlling the membrane potential of individual elements of its presynaptic input ensemble. The membrane potential in the terminals of the presynaptic neuron is composed of two components, graded membrane potential changes and action potentials. To dissociate the roles of action potentials and graded potential changes in synaptic transmission we used voltage-clamp-controlled current-clamp techniques to suppress the graded membrane potential changes without affecting action potentials. Our results indicate that both the graded potential and the action potentials of the presynaptic neuron have an impact on the spiking characteristics of the postsynaptic neuron. Although a tight temporal coupling between pre- and postsynaptic spikes exists, the timing between these spikes is also affected by graded potential changes. We propose that the control of synaptic transfer of a dynamically complex signal by graded changes in membrane potential and spikes is useful to enable a temporally precise coupling of spikes in response to sudden transitions in stimulus intensity.