Moving background patterns reveal double-opponency of directionally specific pigeon tectal neurons

Abstract

The experiments reported in this paper were carried out to determine the effect moving background patterns have on the response characteristics of directionally specific neurons in the pigeon optic tectum. First, care was taken to select the optimal single stimulus for each cell, then large textured patterns were added to the test stimulus and moved either "in-phase" or "anti-phase". Altogether 214 cells were studied in 77 white Carneaux pigeons and it was found that all cells below a depth of 400 microns were inhibited by backgrounds moved "in-phase" with the optimal test stimulus, while few cells above this level were affected in any way by backgrounds. All directions of background motion containing an "in-phase" vector resulted in rather profound inhibition of the directional response while directions with an "anti-phase" vector produced less inhibition and sometimes were even facilitated by direct "anti-phase". The velocity tuning curves obtained with an optimal single test stimulus and by "anti-phase" movement of backgrounds were essentially similar. "In-phase" inhibition can also be produced by a second spot stimulus located some distance from the test stimulus. This latter effect was used to map the outer margins of the inhibitory receptive fields of deep tectal neurons displaying these effects and it was found they were extremely large, often in excess of 100 degrees in diameter. When masks were used to prevent the moving background from stimulating the excitatory receptive field "anti-phase" movement always produced facilitation. This suggests a double opponent-process directionally specific receptive field organization. These neurons seem well suited to respond to local (object) motion and to ignore translation of the visual image arising from body, head and eye movements.

Biological image motion processing: A review

“…To localize these velocity-defined "edges" they proposed the existence of concentrically organized receptive fields having a center-surround antagonism with respect to a particular velocity direction. Such units have been reported for many species (Sterling and Wickeigren, 1969;Collett, 1972;Bridgeman, 1972;Frost, 1978;Frost et al. 1981).…”

Stimulus-Specific Adaptation: Can It Be a Neural Correlate of Behavioral Habituation?

“…Substantial evidence supports the notion that the OT (and its mammalian homolog, the superior colliculus) contains the circuitry to represent the saliency of the incoming stimuli, a prerequisite for selective attention (Ingle, 1975;Frost et al, 1981;Basso and Wurtz, 1997;McPeek and Keller, 2002;Khanbabaie et al, 2007;Boehnke and Munoz, 2008;Mysore et al, 2010). An important element in stimulus saliency is its history.…”

Processing of figure and background motion in the visual system of the fly

“…Collett 1971;Collett and King 1975;Olberg 1981Olberg , 1986Palka 1972;Rowell et al 1977) and vertebrates (e.g. Frost et al 1981;von Griinau and Frost 1983;Allman et al 1985;Tanaka et al 1986). This difference might be due to different behavioral contexts in which small objects moving relative to the eyes have to be detected and our, apart from few examples, complete lack of knowledge in this respect.…”

“…For instance, cells in both area MT in the monkey (e.g. Allman et al 1985) and the optic tectum of the pigeon (Frost et al 1981;Frost and Nakayama 1983) are influenced from beyond their classical excitatory receptive field. These areas can cover considerable parts of the visual field.…”