Biology subjects

Malevich, T.

Publications and source records attributed to Malevich, T..

13 recordsLinked to original sources

bioRxiv2026

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

Optimal behavior requires active coordination between exogenous sensory events and internal brain states. Understanding such coordination is rendered challenging given the massive parallelism, followed by equally massive convergence, of sensory signals, even within a single sensory modality, when conveying information to the motor periphery. Here, using audiovisual stimulation and saccadic orienting, we show how multisensory stimulation differentially recruits visual processing pathways bypassing the primary visual cortex (V1), which may otherwise appear dormant. We reversibly inactivated primate V1 and explored the influences on short-latency reflexive saccadic resetting. Having recently shown that such resetting is eliminated by V1 inactivation, randomly interleaving task-irrelevant simultaneous sounds not only recovered the phenomenon, but it was also associated with V1-independent neuronal modulations in both the superior (SC) and inferior (IC) colliculi. These results show that even when the geniculostriate pathway is dominant, like in primates, alternative visual pathways still alter behavior under the right sensory contingencies.

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bioRxiv2026

Much stronger coarse-to-fine visual processing in primate superior colliculus than primary visual cortex neurons

The visual system optimizes its signal processing properties to efficiently encode natural scenes. The superior colliculus (SC) and primary visual cortex (V1) both play important roles in visual-motor processing, and they both exhibit qualitatively similar visual responses. However, it is not clear whether the SC simply inherits V1s efficient coding image processing optimizations or not, especially given that the SC receives a substantial amount of direct anatomical inputs from V1. Here, by performing matched experiments in the two brain areas, as well as with the same visual stimuli and in the same experimental animals, we show that the dynamics of coarse-to-fine visual image processing in the SC are much stronger than those in V1. In the SC, visual response latencies, being fastest for coarse patterns, are dictated by image spatial frequency, independently of the spatial frequency tuning curves of the neurons. On the other hand, V1 visual response latencies are largely dominated by visual response sensitivity, which is itself much more broadband than in the SC. These observations remain fundamentally unchanged in active vision gaze-shift scenarios eliciting visual reafferent responses in both brain areas. Our results suggest that coarse-to-fine visual image processing dynamics are most observable, and thus most relevant, in visually-responsive neurons driving foveating eye movements, like in the SC. Besides explaining behavioral evidence for saccadic facilitation by images that are consistent with the statistics of natural scenes, these results indicate that coarse-to-fine visual processing dynamics are much more of a collicular than a cortical visual phenomenon.

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bioRxiv2026

Transient focal inactivation of the primary visual cortex abolishes saccadic inhibition

Most organisms are perpetually engaged in an active-perception cycle: at any moment, planning, executing, or recovering from a given own movement. In the oculomotor system, such a cycle is under a powerful, reflexive, and short-latency interruptive influence by exogenous sensory stimulation, but the multitude of possible pathways eventually converging on the final oculomotor control gateway make it unknown how reflexive oculomotor inhibition takes place. Here we show that transient focal inactivation of the primary visual cortex abolishes visually-driven saccadic inhibition, suggesting an unequivocal dominance of the geniculostriate visual pathway over this robust behavioral reflex. Using chronic lesions, computational modeling, and fine-grained eye-movement analyses, we then show that latent visual signals bypassing the geniculostriate pathway are still present, but may not be as central as previously anticipated. These results recast classic views on visual-motor reflexes, and motivate functional and theoretical investigations of the multiplicity of parallel input-output loops in the brain.

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bioRxiv2025

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

Visual onsets in the environment cause a short-latency reduction in saccade generation likelihood. Concomitant with that, the metrics of the saccades that do happen near the time of saccadic inhibition reflect the landscape of stimulus-driven neural responses in topographically organized brain maps. While certain aspects of saccadic inhibition have already been explored from a neurophysiological perspective, several questions remain, including which sensory-motor pathways propagate visual input information to the final oculomotor control circuitry with such short latencies. Here, motivated by evidence of a dissociation between temporal and spatial aspects of saccadic inhibition, we devised behavioral paradigms experimentally manipulating either aspect. Rhesus macaque monkeys maintained gaze fixation, and we characterized visually-driven microsaccadic inhibition with and without paired auditory pulses. In one condition, the sound pulses were spatially-nonlateralized, thus only affecting the temporal processes associated with microsaccadic inhibition; in another, the pulses were spatially-lateralized, affecting both the temporal and spatial components. We found that sound pulses alone barely affected microsaccade rates. However, when paired with visual stimuli, they accelerated the timing of visually-driven microsaccadic inhibition by [~]14-18 ms. In terms of microsaccade directions, spatially-nonlateralized sounds interfered with, but did not eliminate, visually-driven direction modulations. Surprisingly, lateralized sounds had a much weaker effect on microsaccade direction modulations, even when the sound source was in the opposite hemifield as the appearing visual stimulus. We conclude that vision dominates sound in mediating classic microsaccadic inhibition, and we argue that our paradigms are ideal for neurophysiological investigations of the parallel sensory-motor pathways contributing to such inhibition. SignificanceCoordination of internal oculomotor eye movement plans with exogenous sensory events entails rapid inhibition of the saccadic eye movement system, but the pathways mediating the inhibition are unknown. We devised novel behavioral paradigms in primates, involving multisensory stimulation, which allow neurophysiological experiments to isolate the contributions of individual sensory, motor, and sensory-motor brain areas to saccadic inhibition. Such paradigms underscore that inhibition involves distinct temporal and spatial processes that are dominated by the visual modality.

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bioRxiv2025

Much higher covariation with foveation timing by superior colliculus than primary visual cortical neuronal activity

The superior colliculus (SC) is a potent driver for orienting movements, but it also possesses short-latency visual responses. Even though such responses largely derive from direct primary visual cortical (V1) input, their relationship to V1 activity has never been analyzed with the same experimental subjects and stimuli. Here, we revisited pioneering observations that trial-by-trial variability in either SC or V1 visual responses may predict eye movement timing variability. We found that V1 covariation with behavioral variability was virtually non-existent in comparison to the SC, whether with respect to visual response onset latency, visual response strength, or pre-stimulus state. By far, our largest predictor of behavioral variability was visual response strength in SC visual-motor neurons. These results suggest that the SC reformats its sensory inputs for exploitation of the SCs proximity to the motor periphery; V1 aids in jumpstarting the sensing process, but the SC much more directly supports visually-driven orienting.

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bioRxiv2025

Species-specific oculomotor control tolerances predict saccadic suppression strength in macaques and zebrafish

Active sensing necessarily requires integrating information about both self-generated movements as well as past, present, and future afferent inputs. However, such information is inherently variable and relies, at least in part, on uncertain extrapolations. Here, using saccadic suppression of visual sensitivity as a classic example of sensory-motor integration, we show that suppression strength in two drastically different species, macaque monkeys and zebrafish larvae, may be a direct outcome of efficient state estimation in the presence of uncontrollable sensory and motor variability. Bayesian estimator models suggest that optimal saccadic suppression should rely not just on the sensory-motor information being processed, but also on the time-dependent magnitude of unexplained variability in the nervous system encoding it. In both macaques and zebrafish larvae, and using matching visual stimulation regimes optimized for each species receptive field properties, we experimentally measured saccadic suppression strength in the superior colliculus (SC) of the monkeys and the homologous optic tectum (OT) of the fish. We also experimentally quantified additive and multiplicative motor noise components in the oculomotor behavior of both species, and we furthermore estimated noise in the sensory systems. We found that inter-species differences in sensory and motor noise levels and their theoretically predicted impacts on visual sensitivity are consistent with our experimentally observed differences in saccadic suppression strength between the fish and the monkeys. Because sensory and motor noise levels can reflect the amounts of available neural resources committed to a given task, our results strongly underscore the value of incorporating computational resource limits into investigating performance differences that have evolved in homologous brain areas.

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bioRxiv2024

Foveal action for the control of extrafoveal vision

Microsaccades have been convincingly linked to extrafoveal covert attention shifts for more than two decades. However, the direction of causality between individual microsaccade generation and an alteration in both extrafoveal visual sensitivity and behavior remains debated: do microsaccades merely reflect, perhaps probabilistically, an altered extrafoveal sensitivity, or is the act of generating microsaccades sufficient, on its own, to modify such sensitivity? Using a novel exploitation of real-time retinal image stabilization, behavior, and neurophysiology in the superior colliculus of rhesus macaque monkeys, we show that exclusive experimental control over foveal oculomotor state is entirely sufficient to influence extrafoveal sensitivity. This happens for eccentricities as large as [~]50 times those associated with microsaccades, and it also takes place in the absence of any differential attentional demands. Most importantly, such influence is mediated through well-known, classic pre- and post-saccadic visual processing changes. Thus, seemingly-innocuous subliminal eye movements do constitute an integral component of cognitive processes like attention.

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bioRxiv2023

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

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. SignificanceDuring gaze fixation, the eye drifts slowly in between microsaccades. While eye position drifts are generally considered to be random eye movements, we recently found that they are modulated with very short latencies by some stimulus onsets. Here we characterized the feature-tuning properties of such stimulus-driven drift responses. Our results demonstrate that drift eye movements are not random, and that visual stimuli can impact them in a manner similar to how such stimuli impact microsaccades.

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bioRxiv2023

Visual feature tuning properties of stimulus-driven saccadic inhibition in macaque monkeys

Saccadic inhibition refers to a short-latency transient cessation of saccade generation after visual sensory transients. This oculomotor phenomenon occurs with a latency that is consistent with a rapid influence of sensory responses, such as stimulus-induced visual bursts, on oculomotor control circuitry. However, the neural mechanisms underlying saccadic inhibition are not well understood. Here, we exploited the fact that macaque monkeys experience robust saccadic inhibition to test the hypothesis that inhibition time and strength exhibit systematic visual feature tuning properties to a multitude of visual feature dimensions commonly used in vision science. We measured saccades in three monkeys actively controlling their gaze on a target, and we presented visual onset events at random times. Across six experiments, the visual onsets tested size, spatial frequency, contrast, motion direction, and motion speed dependencies of saccadic inhibition. We also investigated how inhibition might depend on the behavioral relevance of the appearing stimuli. We found that saccadic inhibition starts earlier, and is stronger, for large stimuli of low spatial frequencies and high contrasts. Moreover, saccadic inhibition timing depends on motion direction, with earlier inhibition systematically occurring for horizontally than for vertically drifting gratings. On the other hand, saccadic inhibition is stronger for faster motions, and when the appearing stimuli are subsequently foveated. Besides documenting a range of feature tuning dimensions of saccadic inhibition on the properties of exogenous visual stimuli, our results establish macaque monkeys as an ideal model system for unraveling the neural mechanisms underlying a highly ubiquitous oculomotor phenomenon in visual neuroscience. New and noteworthyVisual onsets dramatically reduce saccade generation likelihood with very short latencies. Such latencies suggest that stimulus-induced visual responses, normally jumpstarting perceptual and scene analysis processes, can also directly impact the decision of whether to generate saccades or not, causing saccadic inhibition. Consistent with this, we found that changing the appearance of the visual onsets systematically alters the properties of saccadic inhibition. These results constrain neurally-inspired models of coordination between saccade generation and exogenous sensory stimulation.

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bioRxiv2022

Faster detection of "darks" than "brights" by monkey superior colliculus neurons

Visual processing is segregated into ON and OFF channels as early as in the retina, and the superficial (output) layers of the primary visual cortex are dominated by neurons preferring dark stimuli. However, it is not clear how the timing of neural processing differs between "darks" and "brights" in general, especially in light of psychophysical evidence; it is also equally not clear how subcortical visual pathways that are critical for active orienting represent stimuli of positive (luminance increments) and negative (luminance decrements) contrast polarity. Here, we recorded from all visually-responsive neuron types in the superior colliculus (SC) of two male rhesus macaque monkeys. We presented a disc (0.51 deg radius) within the response fields (RFs) of neurons, and we varied, across trials, stimulus Weber contrast relative to a gray background. We also varied contrast polarity. There was a large diversity of preferences for darks and brights across the population. However, regardless of individual neural sensitivity, most neurons responded significantly earlier to dark than bright stimuli. This resulted in a dissociation between neural preference and visual response onset latency: a neuron could exhibit a weaker response to a dark stimulus than to a bright stimulus of the same contrast, but it would still have an earlier response to the dark stimulus. Our results highlight an additional candidate visual neural pathway for explaining behavioral differences between the processing of darks and brights, and they demonstrate the importance of temporal aspects in the visual neural code for orienting eye movements. Significance statementObjects in our environment, such as birds flying across a bright sky, often project shadows (or images darker than the surround) on our retina. We studied how primate superior colliculus (SC) neurons visually process such dark stimuli. We found that the overall population of SC neurons represented both dark and bright stimuli equally well, as evidenced by a relatively equal distribution of neurons that were either more or less sensitive to darks. However, independent of sensitivity, the great majority of neurons detected dark stimuli earlier than bright stimuli, evidenced by a smaller response latency for the dark stimuli. Thus, SC neural response latency can be dissociated from response sensitivity, and it favors the faster detection of dark image contrasts.

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bioRxiv2021

Saccades along spatial neural circuit discontinuities

Saccades are realized by six extraocular muscles that define the final reference frame for eyeball rotations. However, upstream of the nuclei innervating the eye muscles, eye movement commands are represented in two-dimensional retinocentric coordinates, as is the case in the superior colliculus (SC). In such spatial coordinates, the horizontal and vertical visual field meridians, relative to the line of sight, are associated with neural tissue discontinuities due to routing of binocular retinal outputs when forming retinotopic sensory-motor maps. At the level of the SC, a functional discontinuity along the horizontal meridian was additionally discovered, beyond the structural vertical discontinuity associated with hemifield lateralization. How do such neural circuit discontinuities influence purely cardinal saccades? Using thousands of saccades from 3 rhesus macaque monkeys and 14 human subjects, we show how the likelihood of purely horizontal or vertical saccades is infinitesimally small, nulling a discontinuity problem. This does not mean that saccades are sloppy. On the contrary, saccades exhibit remarkable direction and amplitude corrections to account for small initial eye position deviations due to fixational variability: "purely" cardinal saccades can deviate, with an orthogonal component of as little as 0.03 deg, to correct for tiny target position deviations from initial eye position. In humans, probing perceptual target localization additionally revealed that saccades show different biases from perception when targets deviate slightly from purely cardinal directions. These results demonstrate a new functional role for fixational eye movements in visually-guided behavior, and they motivate further neurophysiological investigations of saccade trajectory control in the brainstem. New and NoteworthyPurely cardinal saccades are often characterized as being straight. We show how a small amount of curvature is inevitable, alleviating an implementational problem of dealing with neural circuit discontinuities in the representations of the visual meridians. The small curvature functionally corrects for minute variability in initial eye position due to fixational eye movements. Saccades are far from sloppy; they deviate by as little as <1% of the total vector size to adjust their landing position.

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bioRxiv2020

Dependence of the stimulus-driven microsaccade rate signature on visual stimulus polarity

Microsaccades have a steady rate of occurrence during maintained gaze fixation, which gets transiently modulated by abrupt sensory stimuli. Such modulation, characterized by a rapid reduction in microsaccade frequency followed by a stronger rebound phase of high microsaccade rate, is often described as the microsaccadic rate signature, owing to its stereotyped nature. Here we investigated the impacts of stimulus polarity (luminance increments or luminance decrements relative to background luminance) and size on the microsaccadic rate signature. We presented brief visual flashes consisting of large or small white or black stimuli over an otherwise gray image background. Both large and small stimuli caused robust early microsaccadic inhibition, but only small ones caused a subsequent increase in microsaccade frequency above baseline microsaccade rate. Critically, small black stimuli were always associated with stronger modulations in microsaccade rate after stimulus onset than small white stimuli, particularly in the post-inhibition rebound phase of the microsaccadic rate signature. Because small stimuli were also associated with expected direction oscillations to and away from their locations of appearance, these stronger rate modulations in the rebound phase meant higher likelihoods of microsaccades opposite the black flash locations relative to the white flash locations. Our results demonstrate that the microsaccadic rate signature is sensitive to stimulus polarity, and they point to dissociable neural mechanisms underlying early microsaccadic inhibition after stimulus onset and later microsaccadic rate rebound at longer times thereafter. These results also demonstrate early access of oculomotor control circuitry to sensory representations, particularly for momentarily inhibiting saccade generation. New and noteworthyMicrosaccades are small saccades that occur during gaze fixation. Microsaccade rate is transiently reduced after sudden stimulus onsets, and then strongly rebounds before returning to baseline. We explored the influence of stimulus polarity (black versus white) on this "rate signature". We found that small black stimuli cause stronger microsaccadic modulations than white ones, but primarily in the rebound phase. This suggests dissociated neural mechanisms for microsaccadic inhibition and subsequent rebound in the microsaccadic rate signature.

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bioRxiv2020

Rapid stimulus-driven modulation of slow ocular position drifts

The eyes are never still during maintained gaze fixation. When microsaccades are not occurring, ocular position exhibits continuous slow changes, often referred to as drifts. Unlike microsaccades, drifts remain to be viewed as largely random eye movements. Here we found that ocular position drifts can, instead, be very systematically stimulus-driven, and with very short latencies. We used highly precise eye tracking in three well trained macaque monkeys and found that even fleeting (~8 ms duration) stimulus presentations can robustly trigger transient and stimulus-specific modulations of ocular position drifts, and with only approximately 60 ms latency. Such drift responses are binocular, and they are most effectively elicited with large stimuli of low spatial frequency. Intriguingly, the drift responses exhibit some image pattern selectivity, and they are not explained by convergence responses, pupil constrictions, head movements, or starting eye positions. Ocular position drifts have very rapid access to exogenous visual information.

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