Visual Feature Tuning Properties of Short-Latency Stimulus-Driven Ocular Position Drift Responses during Gaze Fixation

Abstract

Ocular position drifts during gaze fixation are significantly less well-understood than microsaccades. We recently identified a short-latency ocular position drift response, of approximately 1 min arc amplitude, that is triggered within <100 ms by visual onsets. This systematic eye movement response is feature-tuned and seems to be coordinated with a simultaneous resetting of the saccadic system by visual stimuli. However, much remains to be learned about the drift response, especially for designing better-informed neurophysiological experiments unraveling its mechanistic substrates. Here we systematically tested multiple new feature tuning properties of drift responses. Using highly precise eye tracking in three male rhesus macaque monkeys, we found that drift responses still occur for tiny foveal visual stimuli. Moreover, the responses exhibit size tuning, scaling their amplitude (both up and down) as a function of stimulus size, and they also possess a monotonically increasing contrast sensitivity curve. Importantly, short-latency drift responses still occur for small peripheral visual targets, which additionally introduce spatially-directed modulations in drift trajectories towards the appearing peripheral stimuli. Drift responses also remain predominantly upward even for stimuli exclusively located in the lower visual field, and even when starting gaze position is upward. When we checked the timing of drift responses, we found that it was better synchronized to stimulus-induced saccadic inhibition than to stimulus onset. These results, along with a suppression of drift response amplitudes by peri-stimulus saccades, suggest that drift responses reflect the rapid impacts of short-latency and feature-tuned visual neural activity on final oculomotor control circuitry in the brain.Significance statementDuring gaze fixation, the eye drifts slowly in between microsaccades. While eye position drifts are not entirely random, they remain to be significantly more enigmatic than microsaccades, and they are typically mathematically modeled as random walk processes. Having recently found that these eye movements are systematically modulated with very short latencies by some stimulus onsets, here we characterized the feature-tuning properties of such stimulus-driven drift responses. Our results suggest that drift eye movements reflect the impacts of short-latency sensory signals on the oculomotor system. These results also demonstrate that visual stimuli can impact drift eye movements in a manner similar to how such stimuli impact microsaccades.

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…It is also interesting to note here that there were barely any downward microsaccades in our data at all (Fig. 2); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions (Goffart, Hafed, & Krauzlis, 2012; Goffart, Quinet, Chavane, & Masson, 2006; Khademi et al, 2024; Malevich, Buonocore, & Hafed, 2020; Snodderly, 1987; White, Sparks, & Stanford, 1994; Willeke, Cardenas, Bellet, & Hafed, 2022; Zelinsky, 1996).…”

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…It is also interesting to note here that there were barely any downward microsaccades in our data at all (Fig. 2); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions (Goffart, Hafed, & Krauzlis, 2012; Goffart, Quinet, Chavane, & Masson, 2006; Khademi et al, 2024; Malevich, Buonocore, & Hafed, 2020; Snodderly, 1987; White, Sparks, & Stanford, 1994; Willeke, Cardenas, Bellet, & Hafed, 2022; Zelinsky, 1996).…”

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…All of these observations led us to focus our remaining analyses on predominantly horizontal eye movements with an absolute direction from horizontal of less than 45 deg; we obtained generally similar results when we included all trials into the analyses, as expected given the large number of predominantly horizontal movements seen in Figure 3 . It is also interesting to note here that there were barely any downward microsaccades in our data at all ( Figure 3 ); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions ( Goffart, Hafed, & Krauzlis, 2012 ; Goffart, Quinet, Chavane, & Masson, 2006 ; Khademi et al., 2024 ; Malevich, Buonocore, & Hafed, 2020 ; Snodderly, 1987 ; White, Sparks, & Stanford, 1994 ; Willeke, Cardenas, Bellet, & Hafed, 2022 ; Zelinsky, 1996 ).…”

Sound unmasks short-latency tectal visual signals that are independent of the primary visual cortex

“…Another potential research direction opened by our studies is to examine other reflexive oculomotor behaviors, such as sensory-driven pupil dynamics, as well as the short-latency ocular position drift response 76,77 . Both phenomena may involve neural circuits distinct from those underlying saccadic inhibition.…”

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…It is also interesting to note here that there were barely any downward microsaccades in our data at all (Fig. 2); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions (Goffart, Hafed, & Krauzlis, 2012; Goffart, Quinet, Chavane, & Masson, 2006; Khademi et al, 2024; Malevich, Buonocore, & Hafed, 2020; Snodderly, 1987; White, Sparks, & Stanford, 1994; Willeke, Cardenas, Bellet, & Hafed, 2022; Zelinsky, 1996).…”

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…All of these observations led us to focus our remaining analyses on predominantly horizontal eye movements with an absolute direction from horizontal of less than 45 deg; we obtained generally similar results when we included all trials into the analyses, as expected given the large number of predominantly horizontal movements seen in Figure 3 . It is also interesting to note here that there were barely any downward microsaccades in our data at all ( Figure 3 ); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions ( Goffart, Hafed, & Krauzlis, 2012 ; Goffart, Quinet, Chavane, & Masson, 2006 ; Khademi et al., 2024 ; Malevich, Buonocore, & Hafed, 2020 ; Snodderly, 1987 ; White, Sparks, & Stanford, 1994 ; Willeke, Cardenas, Bellet, & Hafed, 2022 ; Zelinsky, 1996 ).…”

Sound unmasks short-latency tectal visual signals that are independent of the primary visual cortex

“…Another potential research direction opened by our studies is to examine other reflexive oculomotor behaviors, such as sensory-driven pupil dynamics, as well as the short-latency ocular position drift response 76,77 . Both phenomena may involve neural circuits distinct from those underlying saccadic inhibition.…”

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…It is also interesting to note here that there were barely any downward microsaccades in our data at all (Fig. 2); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions (Goffart, Hafed, & Krauzlis, 2012; Goffart, Quinet, Chavane, & Masson, 2006; Khademi et al, 2024; Malevich, Buonocore, & Hafed, 2020; Snodderly, 1987; White, Sparks, & Stanford, 1994; Willeke, Cardenas, Bellet, & Hafed, 2022; Zelinsky, 1996).…”

Microsaccadic suppression of peripheral perceptual detection performance as a function of foveated visual image appearance

“…All of these observations led us to focus our remaining analyses on predominantly horizontal eye movements with an absolute direction from horizontal of less than 45 deg; we obtained generally similar results when we included all trials into the analyses, as expected given the large number of predominantly horizontal movements seen in Figure 3 . It is also interesting to note here that there were barely any downward microsaccades in our data at all ( Figure 3 ); this might be related to general tendencies of the oculomotor system to bias gaze upward, whether in visual or memory conditions ( Goffart, Hafed, & Krauzlis, 2012 ; Goffart, Quinet, Chavane, & Masson, 2006 ; Khademi et al., 2024 ; Malevich, Buonocore, & Hafed, 2020 ; Snodderly, 1987 ; White, Sparks, & Stanford, 1994 ; Willeke, Cardenas, Bellet, & Hafed, 2022 ; Zelinsky, 1996 ).…”

Sound unmasks short-latency tectal visual signals that are independent of the primary visual cortex

“…Another potential research direction opened by our studies is to examine other reflexive oculomotor behaviors, such as sensory-driven pupil dynamics, as well as the short-latency ocular position drift response 76,77 . Both phenomena may involve neural circuits distinct from those underlying saccadic inhibition.…”