Visual feature tuning properties of short-latency stimulus-driven ocular position drift responses during gaze fixation

Abstract

Ocular position drifts during gaze fixation are generally considered to be random walks. However, 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 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 timing 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.

Transient focal inactivation of the primary visual cortex abolishes saccadic inhibition

“…On the other hand, deficits in area 17 of the cat were less complete (149). It would be interes*ng in the future to inves*gate whether V1 inac*va*on, like in our experiments, also eliminates the even smaller ocular dril responses recently described in monkeys (150,151), which also have very short latencies from s*mulus onset. In all, our results recast some classic views on interpre*ng even the most reflexive of oculomotor behaviors, and they mo*vate further pathway inves*ga*ons ul*mately leading to eye muscle control.…”

Transient focal inactivation of the primary visual cortex abolishes saccadic inhibition

“…On the other hand, deficits in area 17 of the cat were less complete (149). It would be interes*ng in the future to inves*gate whether V1 inac*va*on, like in our experiments, also eliminates the even smaller ocular dril responses recently described in monkeys (150,151), which also have very short latencies from s*mulus onset. In all, our results recast some classic views on interpre*ng even the most reflexive of oculomotor behaviors, and they mo*vate further pathway inves*ga*ons ul*mately leading to eye muscle control.…”

Vision dominates sound in mediating classic cue-induced microsaccadic eye movement modulations in rhesus macaque monkeys

“…2. We found that pres+mulus microsaccade direc+ons could indeed exhibit idiosyncra+c biases in individual monkeys, like in humans (87), and which likely reflect biases in ocular drid direc+ons (10,11). To demonstrate this, we split trials according to the visual field loca+on of the visual s+mulus, and we also split the observed microsaccades within each group of trials according to whether they were rightward or ledward in direc+on.…”

“…Thus, we asked whether the generally weaker cueing effects for monkey A (with or without the spa+ally-nonlateralized sounds) could have been related to poten+al hemifield asymmetries in this monkey's microsaccades. We found that pres+mulus microsaccade direc+ons could indeed exhibit idiosyncra+c biases in individual monkeys, like in humans (70), and which likely reflect biases in ocular drie direc+ons (10,11). To demonstrate this, we split trials according to the visual field loca+on of the visual s+mulus, and we also split the observed microsaccades within each group of trials according to whether they were rightward or leeward in direc+on.…”

“…We were motivated by the question of how (micro)saccadic inhibition, and related ocular drift phenomena (10, 11), might be mediated in the brain. Clearly, sensory information needs to arrive at the final oculomotor control pathways with very short latencies, since measurable changes in eye movements can occur as early as 50-100 ms after sensory stimulus onset.…”

“…Sensory transients in the environment have a powerful, unavoidable impact on the oculomotor system, and one that precedes even reflexive orienting responses towards such transients (1). This sensory-driven impact manifests itself as a robust, short-latency modulation not only of saccades (2–5) and microsaccades (6–9), but also of slow ocular position drifts during fixation, which are on the scale of approximately 1 min arc eye movements (10, 11), as well as smooth pursuit (12–14).…”

Transient focal inactivation of the primary visual cortex abolishes saccadic inhibition

“…On the other hand, deficits in area 17 of the cat were less complete (149). It would be interes*ng in the future to inves*gate whether V1 inac*va*on, like in our experiments, also eliminates the even smaller ocular dril responses recently described in monkeys (150,151), which also have very short latencies from s*mulus onset. In all, our results recast some classic views on interpre*ng even the most reflexive of oculomotor behaviors, and they mo*vate further pathway inves*ga*ons ul*mately leading to eye muscle control.…”

Vision dominates sound in mediating classic cue-induced microsaccadic eye movement modulations in rhesus macaque monkeys

“…2. We found that pres+mulus microsaccade direc+ons could indeed exhibit idiosyncra+c biases in individual monkeys, like in humans (87), and which likely reflect biases in ocular drid direc+ons (10,11). To demonstrate this, we split trials according to the visual field loca+on of the visual s+mulus, and we also split the observed microsaccades within each group of trials according to whether they were rightward or ledward in direc+on.…”

“…Thus, we asked whether the generally weaker cueing effects for monkey A (with or without the spa+ally-nonlateralized sounds) could have been related to poten+al hemifield asymmetries in this monkey's microsaccades. We found that pres+mulus microsaccade direc+ons could indeed exhibit idiosyncra+c biases in individual monkeys, like in humans (70), and which likely reflect biases in ocular drie direc+ons (10,11). To demonstrate this, we split trials according to the visual field loca+on of the visual s+mulus, and we also split the observed microsaccades within each group of trials according to whether they were rightward or leeward in direc+on.…”

“…We were motivated by the question of how (micro)saccadic inhibition, and related ocular drift phenomena (10, 11), might be mediated in the brain. Clearly, sensory information needs to arrive at the final oculomotor control pathways with very short latencies, since measurable changes in eye movements can occur as early as 50-100 ms after sensory stimulus onset.…”

“…Sensory transients in the environment have a powerful, unavoidable impact on the oculomotor system, and one that precedes even reflexive orienting responses towards such transients (1). This sensory-driven impact manifests itself as a robust, short-latency modulation not only of saccades (2–5) and microsaccades (6–9), but also of slow ocular position drifts during fixation, which are on the scale of approximately 1 min arc eye movements (10, 11), as well as smooth pursuit (12–14).…”

Transient focal inactivation of the primary visual cortex abolishes saccadic inhibition

“…On the other hand, deficits in area 17 of the cat were less complete (149). It would be interes*ng in the future to inves*gate whether V1 inac*va*on, like in our experiments, also eliminates the even smaller ocular dril responses recently described in monkeys (150,151), which also have very short latencies from s*mulus onset. In all, our results recast some classic views on interpre*ng even the most reflexive of oculomotor behaviors, and they mo*vate further pathway inves*ga*ons ul*mately leading to eye muscle control.…”

Vision dominates sound in mediating classic cue-induced microsaccadic eye movement modulations in rhesus macaque monkeys

“…2. We found that pres+mulus microsaccade direc+ons could indeed exhibit idiosyncra+c biases in individual monkeys, like in humans (87), and which likely reflect biases in ocular drid direc+ons (10,11). To demonstrate this, we split trials according to the visual field loca+on of the visual s+mulus, and we also split the observed microsaccades within each group of trials according to whether they were rightward or ledward in direc+on.…”

“…Thus, we asked whether the generally weaker cueing effects for monkey A (with or without the spa+ally-nonlateralized sounds) could have been related to poten+al hemifield asymmetries in this monkey's microsaccades. We found that pres+mulus microsaccade direc+ons could indeed exhibit idiosyncra+c biases in individual monkeys, like in humans (70), and which likely reflect biases in ocular drie direc+ons (10,11). To demonstrate this, we split trials according to the visual field loca+on of the visual s+mulus, and we also split the observed microsaccades within each group of trials according to whether they were rightward or leeward in direc+on.…”

“…We were motivated by the question of how (micro)saccadic inhibition, and related ocular drift phenomena (10, 11), might be mediated in the brain. Clearly, sensory information needs to arrive at the final oculomotor control pathways with very short latencies, since measurable changes in eye movements can occur as early as 50-100 ms after sensory stimulus onset.…”

“…Sensory transients in the environment have a powerful, unavoidable impact on the oculomotor system, and one that precedes even reflexive orienting responses towards such transients (1). This sensory-driven impact manifests itself as a robust, short-latency modulation not only of saccades (2–5) and microsaccades (6–9), but also of slow ocular position drifts during fixation, which are on the scale of approximately 1 min arc eye movements (10, 11), as well as smooth pursuit (12–14).…”