Abstract
Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. However, visual sensation is an active process, and if there are any brain areas that ought to be particularly in tune with natural scene statistics, it would be sensory-motor areas critical for guiding behavior. Here we found that the rhesus macaque superior colliculus, a structure instrumental for rapid visual exploration with saccades, detects low spatial frequencies, which are the most prevalent in natural scenes, much more rapidly than high spatial frequencies. Importantly, this accelerated detection happens independently of whether a neuron is more or less sensitive to low spatial frequencies to begin with. At the population level, the superior colliculus additionally over-represents low spatial frequencies in neural response sensitivity, even at near-foveal eccentricities. Thus, the superior colliculus possesses both temporal and response gain mechanisms for efficient gaze realignment in low-spatial-frequency-dominated natural environments.
Highlights
Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment
We randomly varied the spatial frequency of the grating that we presented to a given neuron from trial to trial, and we noticed a systematic rank ordering of neural response latencies as a function of spatial frequency
This is reminiscent of coarse-to-fine image coding properties of early visual areas[11,12,13,14,15], but it still violated an expected inverse relationship between response latency and sensitivity previously reported in the SC26
Summary
Visual brain areas exhibit tuning characteristics well suited for image statistics present in our natural environment. Ecological constraints[6,7,8] on both visual perception and eye movements imply that the primate SC, like other brain regions, should best function if its neurons’ properties were well matched with the properties of the environment Among such properties is the preponderance of low spatial frequencies in natural scene statistics[9,10]. We found that at the population level, macaque SC neural sensitivity to spatial frequency was primarily low-pass in nature, meaning that both SC response time and SC response strength are efficient when visually analyzing the low spatial frequencies that are abundantly present in natural scenes These observations have allowed us to predict, with high fidelity, our animals’ saccadic RT patterns as a function of spatial frequency based solely on SC visual response strength and latency measurements obtained from completely different experimental sessions not involving saccadic responses. We believe that our findings clarify important visual functions of the primate SC[7], complementary to this structure’s more well-studied motor[2] and cognitive[5,23] functions
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