Biology subjects

Hafed, Z. M.

Publications and source records attributed to Hafed, Z. M..

At least 37 records · Page 2Linked to original sources

bioRxiv2022

Sensory tuning in neuronal movement commands

Movement control is critical for successful interaction with our environment. However, movement does not occur in complete isolation of sensation, and this is particularly true of eye movements. Here we show that the neuronal eye movement commands emitted by the superior colliculus, a structure classically associated with oculomotor control, encompass a robust visual sensory representation of eye movement targets. Thus, similar saccades towards different images are associated with different saccade-related "motor" bursts. Such sensory tuning in superior colliculus saccade motor commands appeared for all image manipulations that we tested, from simple visual features to real-life object images, and it was also strongest in the most motor neurons in the deeper collicular layers. Visual-feature discrimination performance in the motor commands was also stronger than in visual responses. Comparing superior colliculus motor command feature discrimination performance to that in the primary visual cortex during steady gaze fixation revealed that collicular motor bursts possess a reliable peri-saccadic sensory representation of the peripheral saccade targets visual appearance, exactly when retinal input is most uncertain. Consistent with this, we found that peri-saccadic perception is altered as a function of saccade target visual features. Therefore, superior colliculus neuronal movement commands likely serve a fundamentally sensory function.

neuroscience↗

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.

neuroscience↗

bioRxiv2022

Peri-saccadic visual sensitivity is higher in the upper visual field

Visual neural processing is distributed among a multitude of sensory and sensory-motor brain areas exhibiting varying degrees of functional specializations and spatial representational anisotropies. Such diversity raises the question of how perceptual performance is determined, at any one moment in time, during natural active visual behavior. Here, exploiting a known dichotomy between the primary visual cortex and superior colliculus in representing either the upper or lower visual fields, we asked whether peri-saccadic orientation identification performance is dominated by one or the other spatial anisotropy. Humans (48 participants, 29 females) reported the orientation of peri-saccadic upper visual field stimuli significantly better than lower visual field stimuli, unlike their performance during steady-state gaze fixation, and contrary to expected perceptual superiority in the lower visual field in the absence of saccades. Consistent with this, peri-saccadic superior colliculus visual neural responses in two male rhesus macaque monkeys were also significantly stronger in the upper visual field than in the lower visual field. Thus, peri-saccadic orientation identification performance is more in line with oculomotor, rather than visual, map spatial anisotropies. Significance statementDifferent brain areas respond to visual stimulation, but they differ in the degrees of functional specializations and spatial anisotropies that they exhibit. For example, the superior colliculus both responds to visual stimulation, like the primary visual cortex, and controls oculomotor behavior. Compared to the primary visual cortex, the superior colliculus exhibits an opposite pattern of upper/lower visual field anisotropy, being more sensitive to the upper visual field. Here, we show that human peri-saccadic orientation identification performance is better in the upper compared to the lower visual field. Consistent with this, monkey superior colliculus visual neural responses to peri-saccadic stimuli follow a similar pattern. Our results indicate that peri-saccadic perceptual performance reflects oculomotor, rather than visual, map spatial anisotropies.

neuroscience↗

bioRxiv2022

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

Visual pattern analysis relies on computations from neurons possessing spatially confined receptive fields. Often, such receptive fields are orders of magnitude larger than the visual pattern components being processed, as well as these components minute displacements on the retina, whether due to small object or self motions. Yet, perception effortlessly handles such visual conditions. Here, we show that in the primate superior colliculus, a brain structure long associated with oculomotor control, neurons with relatively large receptive fields are still sensitive to visual pattern displacements as small as 1 min arc. We used real-time gaze-contingent retinal image stabilization to control the instantaneous spatio-temporal luminance modulation of detailed patterns experienced by neurons, probing sensitivity to the lower limit of natural self-induced image displacements. Despite a large difference between pattern displacement amplitudes and receptive field sizes, collicular neurons were strongly sensitive to the visual pattern consequences of the smallest possible image-shifting eye movements.

neuroscience↗

bioRxiv2022

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

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.

neuroscience↗

bioRxiv2021

Severe distortion in the representation of foveal visual image locations in short term memory

The foveal visual image region provides the human visual system with the highest acuity. However, it is unclear whether such a high fidelity representational advantage is maintained when foveal image locations are committed to short term memory. Here we describe a paradoxically large distortion in foveal target location recall by humans. We briefly presented small, but high contrast, points of light at eccentricities ranging from 0.1 to 12 deg, while subjects maintained their line of sight on a stable target. After a brief memory period, the subjects indicated the remembered target locations via computer controlled cursors. The biggest localization errors, in terms of both directional deviations and amplitude percentage overshoots or undershoots, occurred for the most foveal targets, and such distortions were still present, albeit with qualitatively different patterns, when subjects shifted their gaze to indicate the remembered target locations. Foveal visual images are severely distorted in short term memory.

neuroscience↗

bioRxiv2021

Superior colliculus saccade motor bursts do not dictate movement kinematics

The primate superior colliculus (SC) contains a topographic map of space, such that the anatomical location of active neurons defines a desired eye movement vector. Complementing such a spatial code, SC neurons also exhibit saccade-related bursts that are tightly synchronized with movement onset. Current models suggest that such bursts constitute a rate code dictating movement kinematics. Here, using two complementary approaches, we demonstrate a dissociation between the SC rate code and saccade kinematics. First, we show that SC burst strength systematically varies depending on whether saccades of the same amplitude are directed towards the upper or lower visual fields, but the movements themselves have similar kinematics. Second, we show that for the same saccade vector, when saccades are significantly slowed down by the absence of a visible saccade target, SC saccade-related burst strengths can be elevated rather than diminished. Thus, SC saccade-related motor bursts do not necessarily dictate movement kinematics.

neuroscience↗

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.

neuroscience↗

bioRxiv2020

Dependence of perceptual saccadic suppression on peri-saccadic image flow properties and luminance contrast polarity

Across saccades, perceptual detectability of brief visual stimuli is strongly diminished. We recently observed that this perceptual suppression phenomenon is jumpstarted in the retina, suggesting that the phenomenon might be significantly more visual in nature than normally acknowledged. Here, we explicitly compared saccadic suppression strength when saccades were made across a uniform image of constant luminance versus when saccades were made across image patches of different luminance, width, and trans-saccadic luminance polarity. We measured perceptual contrast thresholds of human subjects for brief peri-saccadic flashes of positive (luminance increments) or negative (luminance decrements) polarity. Perceptual thresholds were >6-7 times higher when saccades translated a luminance stripe or edge across the retina than when saccades were made over a completely uniform image patch. Critically, both background luminance and flash luminance polarity relative to the background strongly modulated peri-saccadic contrast thresholds. In addition, all of these very same visual dependencies also occurred in the absence of any saccades, but with qualitatively similar rapid translations of image patches across the retina. Our results support the notion that perceptual saccadic suppression may be fundamentally a visual phenomenon, and they motivate neurophysiological and theoretical investigations on the role of saccadic eye movement commands in modulating its properties.

neuroscience↗

bioRxiv2020

Retinal mechanisms of saccadic suppression and their role in processing sequential stimuli

Visual perception remains stable across saccadic eye movements, despite the concurrent strongly disruptive visual flow. This stability is partially associated with a reduction in visual sensitivity, known as saccadic suppression, which already starts in the retina with reduced ganglion cell sensitivity. However, the retinal circuit mechanisms giving rise to such suppression remain unknown. Here, we describe these mechanisms using electrophysiology in mouse, pig, and macaque retina, 2-photon calcium imaging, computational modeling, and human psychophysics. We find that sequential stimuli, such as those that naturally occur during saccades, trigger three independent suppressive mechanisms in the retina. The main suppressive mechanism is triggered by contrast-reversing sequential stimuli and originates within the receptive field center of ganglion cells. It does not involve inhibition or other known suppressive mechanisms such as saturation or adaptation. Instead, it relies on temporal filtering of the inherently slow response of cone photoreceptors coupled with downstream nonlinearities. Two further mechanisms of suppression are present predominantly in ON ganglion cells and originate in the receptive field surround, highlighting a novel disparity between ON and OFF ganglion cells. The mechanisms uncovered here likely play a role in shaping the retinal output following eye movements and other natural viewing conditions where sequential stimulation is ubiquitous.

neuroscience↗

bioRxiv2020

Task-irrelevant visual forms facilitate covert and overt spatial selection

Covert and overt spatial selection behaviors are guided by both visual saliency maps derived from early visual features as well as priority maps reflecting high-level cognitive factors. However, whether mid-level perceptual processes associated with visual form recognition contribute to covert and overt spatial selection behaviors remains unclear. We hypothesized that if peripheral visual forms contribute to spatial selection behaviors, then they should do so even when the visual forms are task-irrelevant. We tested this hypothesis in male and female human subjects as well as in male macaque monkeys performing a visual detection task. In this task, subjects reported the detection of a supra-threshold target spot presented on top of one of two peripheral images, and they did so with either a speeded manual button press (humans) or a speeded saccadic eye movement response (humans and monkeys). Crucially, the two images, one with a visual form and the other with a partially phase-scrambled visual form, were completely irrelevant to the task. In both manual (covert) and oculomotor (overt) response modalities, and in both humans and monkeys, response times were faster when the target was congruent with a visual form than when it was incongruent. Importantly, incongruent targets were associated with almost all errors, suggesting that forms automatically captured selection behaviors. These findings demonstrate that mid-level perceptual processes associated with visual form recognition contribute to covert and overt spatial selection. This indicates that neural circuits associated with target selection, such as the superior colliculus, may have privileged access to visual form information. Significance statementSpatial selection of visual information either with (overt) or without (covert) foveating eye movements is critical to primate behavior. However, it is still not clear whether spatial maps in sensorimotor regions known to guide overt and covert spatial selection are influenced by peripheral visual forms. We probed the ability of humans and monkeys to perform overt and covert target selection in the presence of spatially congruent or incongruent visual forms. Even when completely task-irrelevant, images of visual objects had a dramatic effect on target selection, acting much like spatial cues used in spatial attention tasks. Our results demonstrate that traditional brain circuits for orienting behaviors, such as the superior colliculus, likely have privileged access to visual object representations.

neuroscience↗

bioRxiv2020

Instantaneous movement-unrelated midbrain activity modifies ongoing eye movements

At any moment in time, new information is sampled from the environment and interacts with ongoing brain state. Often, such interaction takes place within individual circuits that are capable of both mediating the internally ongoing plan as well as representing exogenous sensory events. Here we investigated how sensory-driven neural activity can be integrated, very often in the same neuron types, into ongoing oculomotor commands for saccades. Despite the ballistic nature of saccades, visually-induced action potentials in the superior colliculus (SC), a structure known to drive eye movements, not only occurred intra-saccadically, but they were also associated with highly predictable modifications of ongoing eye movements. Such predictable modifications reflected a simultaneity of movement-related discharge at one SC site and visually-induced activity at another. Our results suggest instantaneous readout of the SC map during movement generation, irrespective of activity source, and they explain a significant component of kinematic variability of motor outputs.

neuroscience↗

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.

neuroscience↗

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.

neuroscience↗

bioRxiv2019

Visual feature tuning of superior colliculus neural reafferent responses after fixational microsaccades

The primate superior colliculus (SC) is causally involved in microsaccade generation. Moreover, visually-responsive SC neurons across this structures topographic map, even at peripheral eccentricities much larger than the tiny microsaccade amplitudes, exhibit significant modulations of evoked response sensitivity when stimuli appear peri-microsaccadically. However, during natural viewing, visual stimuli are normally stably present in the environment and are only shifted on the retina by eye movements. Here we investigated this scenario for the case of microsaccades, asking whether and how SC neurons respond to microsaccade-induced image jitter. We recorded neural activity from two male rhesus macaque monkeys. Within the response field (RF) of a neuron, there was a stable stimulus consisting of a grating of one of three possible spatial frequencies. The grating was stable on the display, but microsaccades periodically jittered the retinotopic RF location over it. We observed clear short-latency visual reafferent responses after microsaccades. These responses were weaker, but earlier (relative to new fixation onset after microsaccade end), than responses to sudden stimulus onsets without microsaccades. The reafferent responses clearly depended on microsaccade amplitude, as well as microsaccade direction relative to grating orientation. Our results indicate that one way for microsaccades to influence vision is through modulating how the spatio-temporal landscape of SC visual neural activity represents stable stimuli in the environment. Such representation strongly depends on the specific pattern of temporal luminance modulations expected from the relative relationship between eye movement vector (size and direction), on the one hand, and spatial visual pattern layout, on the other. Significance statementDespite being diminutive, microsaccades still jitter retinal images. We investigated how such jitter affects superior colliculus (SC) activity. We found that SC neurons exhibit short-latency visual reafferent bursts after microsaccades. These bursts reflect not only the spatial luminance profiles of visual patterns, but also how such profiles are shifted by eye movement size and direction. These results indicate that the SC continuously represents visual patterns, even as they are jittered by the smallest possible saccades.

neuroscience↗

bioRxiv2019

Gaze direction as equilibrium: more evidence from spatial and temporal aspects of small-saccade triggering in the rhesus macaque monkey

Rigorous behavioral studies made in human subjects have shown that small-eccentricity target displacements are associated with increased saccadic reaction times, but the reasons for this remain unclear. Before characterizing the neurophysiological foundations underlying this relationship between the spatial and temporal aspects of saccades, we tested the triggering of small saccades in the male rhesus macaque monkey. We also compared our results to those obtained in human subjects, both from the existing literature and through our own additional measurements. Using a variety of behavioral tasks exercising visual and non-visual guidance of small saccades, we found that small saccades consistently require more time than larger saccades to be triggered in the non-human primate, even in the absence of any visual guidance and when valid advance information about the saccade landing position is available. We also found a strong asymmetry in the reaction times of small upward versus downward visually-guided saccades, similar to larger saccades, a phenomenon that has not been described before for small saccades, even in humans. Following the suggestion that an eye movement is not initiated as long as the visuo-oculomotor system is within a state of balance, in which opposing commands counterbalance each other, we propose that the longer reaction times are a signature of enhanced times needed to create the symmetry-breaking condition that puts downstream premotor neurons into a push-pull regime necessary for rotating the eyeballs. Our results provide an important catalog of non-human primate oculomotor capabilities on the miniature scale, allowing concrete predictions on underlying neurophysiological mechanisms.

neuroscience↗

bioRxiv2019

Using deep neural networks to detect complex spikes of cerebellar Purkinje Cells

One of the most powerful excitatory synapses in the entire brain is formed by cerebellar climbing fibers, originating from neurons in the inferior olive, that wrap around the proximal dendrites of cerebellar Purkinje cells. The activation of a single olivary neuron is capable of generating a large electrical event, called "complex spike", at the level of the postsynaptic Purkinje cell, comprising of a fast initial spike of large amplitude followed by a slow polyphasic tail of small amplitude spikelets. Several ideas discussing the role of the cerebellum in motor control are centered on these complex spike events. However, these events are extremely rare, only occurring 1-2 times per second. As a result, drawing conclusions about their functional role has been very challenging, as even few errors in their detection may change the result. Since standard spike sorting approaches cannot fully handle the polyphasic shape of complex spike waveforms, the only safe way to avoid omissions and false detections has been to rely on visual inspection of long traces of Purkinje cell recordings by experts. Here we present a supervised deep learning algorithm for rapidly and reliably detecting complex spikes as an alternative to tedious visual inspection. Our algorithm, utilizing both action potential and local field potential signals, not only detects complex spike events much faster than human experts, but it also excavates key features of complex spike morphology with a performance comparable to that of such experts. Significance statementClimbing fiber driven "complex spikes", fired at perplexingly low rates, are known to play a crucial role in cerebellum-based motor control. Careful interpretations of these spikes require researchers to manually detect them, since conventional online or offline spike sorting algorithms (optimized for analyzing the much more frequent "simple spikes") cannot be fully trusted. Here, we present a deep learning approach for identifying complex spikes, which is trained on local field and action potential recordings from cerebellar Purkinje cells. Our algorithm successfully identifies complex spikes, along with additional relevant neurophysiological features, with an accuracy level matching that of human experts, yet with very little time expenditure.

neuroscience↗

bioRxiv2019

Saccadic suppression by way of retinal-circuit image processing

Visual sensitivity, probed through perceptual detectability of very brief visual stimuli, is strongly impaired around the time of rapid eye movements. This robust perceptual phenomenon, called saccadic suppression, is frequently attributed to active suppressive signals that are directly derived from eye movement commands. Here we show instead that visual-only mechanisms, activated by saccade-induced image shifts, can account for all perceptual properties of saccadic suppression that we have investigated. Such mechanisms start at, but are not necessarily exclusive to, the very first stage of visual processing in the brain, the retina. Critically, neural suppression originating in the retina outlasts perceptual suppression around the time of saccades, suggesting that extra-retinal movement-related signals, rather than causing suppression, may instead act to shorten it. Our results demonstrate a far-reaching contribution of visual processing mechanisms to perceptual saccadic suppression, starting in the retina, without the need to invoke explicit motor-based suppression commands.

neuroscience↗