The RF-cinematogram

Abstract

We present a spike-triggered averaging method capable of mapping the visual receptive fields of several neurons simultaneously. The stimulation is general and the mapping proceeds automatically without the need to match the stimulation to the cells' preference for position, orientation, direction, etc. The maps are spatiotemporal; receptive field (RF) structures are quantitatively determined in three dimensions: the two dimensions of visuotopic space, and time. The method presented is one of a family of “reverse correlation” or “spike-triggered averaging” techniques (DeBoer and Kuyper 1968) capable of revealing linear aspects of stimulus-response coupling. The formal relationship of these methods to stimulus-response crosscorrelation is shown. The analysis is extended to provide some second-order axis-of-motion information (“direction marks”). The stimulus is a constantly illuminated, randomly jumping bright or dark spot, not an elongated bar. Spot diameters between one-third to 1 × RF width are effective. The method ascertains for each recorded action potential or “spike” the prior visual field position of the spot. The average or most probable spot positions define the receptive field spatially. Repeating the process for a succession of times prior to observed spikes defines the field temporally, presented here as a succession of spatial maps. We term this portrayal a receptive field cinematogram, RFc or ciné. The RFc reveals and economically portrays the spread of excitability and suppression across the receptive field, culminating in the generation of a spike. RFcs for LGN neurons and for simple cells recorded in cat cortical areas 17 and 18 are presented and interpreted in terms of classic ON/OFF regions. The availability of temporal information permits the separation of an excitatory exit response, generated when a moving bright spot leaves an OFF region, from an excitatory entrance response occurring when a bright spot enters an ON region, because these responses occur at different times (exit responses earlier). Spike emission remains coupled to (cross-correlated with) stimulus events over time periods as long as 96 ms, implying that some stimulus drive or afferent visual input is delayed by as much as 96 ms more than other input. This is a striking instance of temporal dispersion in the visual system. In some cells, said to be “spatiotemporally inseparable”, the delay (latency) varies systematically across the visual field; i.e., the place for optimal stimulation varies with the time prior to spike emission. In these cells, the RFc shows receptive field structures which move across the visual field over trajectories equal to approximately twice the total conventional RF width. Exit and entrance responses, on the other hand, arise in a simple way from separated ON and OFF RF subregions. ON/ OFF mechanisms thus appear unrelated to spatiotemporal inseparability. The RFc method is easily automated, efficient, and characterizes multiple RFs simultaneously, as required in work with multiple electrode arrays.