In Vivo Calcium Accumulation in Presynaptic and Postsynaptic Dendrites of Visual Interneurons

Abstract

In this comparative in vivo study of dendritic calcium accumulation, we describe the time course and spatial integration properties of two classes of visual interneurons in the lobula plate of the blowfly. Calcium accumulation was measured during visual motion stimulation, ensuring synaptic activation of the neurons within their natural spatial and temporal operating range. The compared cell classes, centrifugal horizontal (CH) and horizontal system (HS) cells, are known to receive retinotopic input of similar direction selectivity, but to differ in morphology, biophysics, presence of dendrodendritic synapses, and computational task. 1) The time course of motion-induced calcium accumulation was highly invariant with respect to stimulus parameters such as pattern contrast and size. In HS cells, the rise of [Ca2+]i can be described by a single exponential with a time constant of 5–6 s. The initial rise of [Ca2+]i in CH cells was much faster (τ ≈ 1 s). The decay time constant in both cell classes was estimated to be at least 3.5 times longer than the corresponding rise time constant. 2) The voltage-[Ca2+]i relationship was best described by an expansive nonlinearity in HS cells and an approximately linear relationship in CH cells. 3) Both cell classes displayed a size-dependent saturation nonlinearity of the calcium accumulation. Although in CH cells calcium saturation was indistinguishable from saturation of the membrane potential, saturation of the two response parameters differed in HS cells. 4) There was spatial overlap of the calcium signal in response to nonoverlapping visual stimuli. Both the area and the amplitude of the overlap profile was larger in CH cells than in HS cells. Thus calcium accumulation in CH cells is spatially blurred to a greater extent than in HS cells. 5) The described differences between the two cell classes may reflect the following computational tasks of these neurons: CH cells relay retinotopic information within the lobula plate via dendritic synapses with pronounced spatial low-pass filtering. HS cells are output neurons of the lobula plate, in which the slow, local calcium accumulation may be suitable for local modulatory functions.