Express detection and discrimination of visual objects by primate superior colliculus neurons

Abstract

Primate superior colliculus (SC) neurons exhibit rich visual feature tuning properties and are implicated in a subcortical network hypothesized to mediate fast threat and/or conspecific detection. However, the mechanisms through which generalized object detection may be mediated by SC neurons remain unclear. Here we explored whether, and how quickly, SC neurons detect and discriminate real-life object stimuli. We presented experimentally-controlled gray-scale images of seven different object categories within the response fields (RFs) of SC neurons, and we also presented a variety of luminance- and spectral-matched image controls. We found that all of our functionally-identified SC neuron types preferentially detected real-life objects even in their very first stimulus-evoked visual bursts (starting within approximately 50 ms from image onset). Intriguingly, even visually-responsive motor-related neurons exhibited such robust early object detection, and they also preferentially discriminated between object categories in their initial visual bursts. We further identified spatial frequency information in visual images as a critical source for early object detection and discrimination by SC neurons. Our results demonstrate rapid and robust SC processing of visual objects, and they underline how the visual processing capabilities of the primate SC support perception and action.

Superior colliculus visual neural sensitivity at the lower limit of natural self-induced image displacements

“…Thus, even though SC neurons may have large RF's, they still exhibit sensitivity to highly local image features. This idea is consistent with the notion that the primate SC can contribute to visual scene analysis 4,5,26 and object processing 6,[27][28][29][30] in a variety of ways. Our results are relevant with respect to theoretical predictions on how eye position drifts can reformat visual images by introducing temporal fluctuations of image luminance at any one position on the retina [13][14][15][16]31 .…”

“…Thus, even though SC neurons may have large RF’s, they still exhibit sensitivity to highly local image features. This idea is consistent with the notion that the primate SC can contribute to visual scene analysis 4,5,26 and object processing 6,27-30 in a variety of ways.…”

“…Outside the fovea, and particularly in higher visual areas, RF's can be large. This is also the case in sensory-motor structures like the superior colliculus (SC) [1][2][3] , which itself has a rich and diverse visual repertoire [1][2][3][4][5][6][7] . Integration of relatively large image regions by individual RF's raises questions about how detailed visual pattern analysis can occur when the local features inside an RF are much smaller than RF size.…”

Faster detection of “darks” than “brights” by monkey superior colliculus neurons

“…In all cases, including the single electrode sessions, we also performed offline sorting to re-isolate neurons for inclusion in the data analysis pipeline (Pachitariu et al, 2016). Sorting and general data analysis pipeline details were similar to those described recently (Bogadhi and Hafed, 2022). Before collecting data from our main tasks, we first identified the SC by running RF mapping tasks.…”

“…Eye movements in monkey F were recorded with a video-based eye tracker (EyeLink1000; desktop mount; 1 KHz sampling rate). For the present experiments, monkeys M and A also each had a recording chamber centered on the midline and tilted 38 deg posterior of vertical, allowing access to both the right and left SC (Bogadhi and Hafed, 2022).…”