Abstract
The superficial layers of the superior colliculus (sSC) appear to function as a subcortical visual pathway that bypasses the striate cortex for the rapid processing of coarse facial information. We investigated the responses of neurons in the monkey sSC during a delayed non-matching-to-sample (DNMS) task in which monkeys were required to discriminate among five categories of visual stimuli [photos of faces with different gaze directions, line drawings of faces, face-like patterns (three dark blobs on a bright oval), eye-like patterns, and simple geometric patterns]. Of the 605 sSC neurons recorded, 216 neurons responded to the visual stimuli. Among the stimuli, face-like patterns elicited responses with the shortest latencies. Low-pass filtering of the images did not influence the responses. However, scrambling of the images increased the responses in the late phase, and this was consistent with a feedback influence from upstream areas. A multidimensional scaling (MDS) analysis of the population data indicated that the sSC neurons could separately encode face-like patterns during the first 25-ms period after stimulus onset, and stimulus categorization developed in the next three 25-ms periods. The amount of stimulus information conveyed by the sSC neurons and the number of stimulus-differentiating neurons were consistently higher during the 2nd to 4th 25-ms periods than during the first 25-ms period. These results suggested that population activity of the sSC neurons preferentially filtered face-like patterns with short latencies to allow for the rapid processing of coarse facial information and developed categorization of the stimuli in later phases through feedback from upstream areas.
Highlights
The superior colliculus (SC) is a multilayered structure in the mammalian midbrain
The activity of the neuron increased sharply in response to the onset of the stimuli, decreased rapidly, and gradually increased again. This pattern of changes in neuronal activity formed the following two response phases: an early rapid response phase and a late gradual response phase. This neuron responded differentially to the head orientation of the human photos; the left profiles elicited the strongest responses while this neuron was less sensitive to frontal faces
Distance between the stimuli in the multidimensional scaling (MDS) space in the first epoch in superficial layers of the superior colliculus (sSC) (Figure 9A) was significantly correlated in that in the MDS space in the first epoch in the pulvinar (Pearson’s correlation coefficient; r2 = 0.850, p < 0.001). These results indicated that neuronal response magnitudes and latencies www.frontiersin.org to the visual stimuli in sSC were significantly correlated with those in the pulvinar, and that both sSC and pulvinar represented the visual stimuli in the MDS space
Summary
Its superficial layers (sSC) receive visual inputs from the retina (Leventhal et al, 1981; Perry and Cowey, 1984; Rodieck and Watanabe, 1993). Humans and monkeys with V1 lesions display residual visual functions in the blind area (i.e., blindsight) (Stoerig and Cowey, 1997; Yoshida et al, 2012). Human subjects with V1 lesions can respond differentially to the spatial localization of stationary and moving stimuli (Perenin and Jeannerod, 1975; Blythe et al, 1987), motion direction (Barbur et al, 1980; Perenin, 1991), line orientation (Weiskrantz, 1987), wavelength (Morland et al, 1999), and form (Perenin and Rossetti, 1996)
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