Eye Movements: Neural processes and models

Talk Session: Tuesday, May 23, 2023, 2:30 – 4:15 pm, Talk Room 1
Moderator: Robert McPeek, SUNY

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Talk 1, 2:30 pm, 54.11

Object-based saccadic enhancement of superior colliculus activity

Christopher Conroy¹ (), Hossein Adeli², Abe Leite², Gregory J. Zelinsky², Robert M. McPeek¹; ¹SUNY College of Optometry, ²Stony Brook University

The superior colliculus (SC) plays an important role in the control of visual spatial attention, in particular in situations where such control involves saccades. We wondered if it also plays a role in the control of object-based attention, motivated by the fact that saccades are often directed not simply to locations in space but rather to parts of extended objects. A rhesus monkey was trained to fixate a spot of light and make a saccade to a peripheral cue. On each trial, an extended object was presented along with two stimuli indicating potential saccade goals. The correct saccade goal was randomly selected from the two stimuli and was cued by a subtle spatial extension of its length. In the connected condition, the potential saccade goals were contiguous with the extended object. In the disconnected condition, they were presented at the same spatial locations but were separated from the extended object by a short distance. We recorded from SC neurons that had response fields (RFs) that overlapped the extended object yet were spatially remote from the saccade goals. Thus, in the connected condition, the saccade goal and RF stimulus were part of the same extended object, whereas, in the disconnected condition, they were not. Otherwise, the saccade goals, the saccades that were made, and the RF stimuli were the same. Nevertheless, we found that, around the time of saccade execution, SC activity was enhanced in the connected condition relative to the disconnected condition. This suggests that, during a saccade to an extended object, there is an enhanced representation of that object at the level of the SC. The results, therefore, suggest a potential role for the SC in object- as well as space-based attentional control, at least when the object to be attended is the target of an impending saccade.

Acknowledgements: NIH-NEI R01-EY030669

Talk 2, 2:45 pm, 54.12

Relating trial-to-trial variability in superior colliculus visual responses to saccadic reaction time variability

Carlotta Trottenberg¹ (), Ziad Hafed¹; ¹University of Tübingen

Reflexive saccades towards the same appearing stimulus vary substantially in their reaction times (RT’s). While several cognitive processes, like target selection and decision making, contribute to such variability, none of these processes can begin before sensory detection of stimulus occurrence. Consistent with this, variability in the time at which primary visual cortex (V1) neurons first detect stimulus onset is significantly correlated with RT variability (Lee et al., 2010). We asked how trial-to-trial variability in the visual responses of the superior colliculus (SC), a structure with both visual sensitivity and direct projections to oculomotor control circuitry, behaves. We analyzed recordings of 188 SC neurons from two macaque monkeys that performed a reflexive visually-guided saccade task. After 550-800 ms of initial fixation, a 0.51-deg radius disc of 10-100% contrast appeared within the response field of a neuron; the fixation spot was extinguished simultaneously. We estimated the first-spike latency of visual responses using a similar method to (Lee et al., 2010). We also calculated spike likelihood across trials in 2-ms running time bins. Within a given contrast level, we observed a significant positive correlation between trial-to-trial first-spike latency and RT, like in V1. However, numerically, the correlations were surprisingly weaker than in the V1 data of Lee et al. (2010). We then analyzed spike likelihood in the SC visual responses. In this case, and unlike in V1, trial-to-trial variability in firing rate, again within a given contrast level, exhibited stronger correlations with RT (which were now negative: lower spike rates implying longer RT’s). These results suggest that a rate, rather than temporal, code dominates the relationship between trial-to-trial SC visual response variability and RT’s. We hypothesize that relying on a rate code, necessitating temporal integration, can reduce sensitivity to noise, which can erroneously trigger movements through the SC’s descending brainstem projections.

Talk 3, 3:00 pm, 54.13

Neural subpopulations in marmoset area MTC but not MT show extra-retinal tuning for saccade direction

Amy Bucklaew¹ (), Shanna Coop², Jude Mitchell^1,2; ¹Neuroscience Graduate Program, University of Rochester, ²Brain and Cognitive Sciences, University of Rochester

Previously we found pre-saccadic neural enhancements in two adjacent motion processing areas of the marmoset monkey, middle temporal (MT) and middle temporal crescent (MTC) areas (Bucklaew et al., VSS, 2021). While area MT has been the focus of previous studies much less is known about area MTC, which in macaque corresponds to areas V4t and MST lateral. Area MTC contains a high proportion of neurons selective to stimulus motion and with receptive fields slightly larger than MT (Elston & Rosa, 1999). In the marmoset it is straight-forward to distinguish between these areas based on their retinotopy across successive electrode penetrations. Here we asked if the two areas differ based on how they integrate extra-retinal feedback during saccades. We recorded from neurons in both areas as two monkeys freely viewed either natural images or a blank screen. For natural images we observe that MT neurons show classic patterns of saccadic suppression around saccade onset followed by a post-saccadic increase 50% over baseline after 50ms. By contrast, for blank backgrounds MT neurons show less than 10% modulation for either suppression or post-saccadic increases. Area MTC differed from MT in that the early response interval (<50ms) showed a distinct peak rather than suppression. There was on average a 54% early increase with natural images, and that increase remained significant for blank backgrounds. This early peak in response likely reflects an extra-retinal feedback to MTC. We found that the early peak was driven by a subpopulation of cells (24%) that had strong modulations (50% or greater) and that showed significant tuning for the direction of saccade. This suggests that area MTC differs from MT in that it receives extra-retinal feedback about the direction of saccades.

Acknowledgements: AB, SC, and JFM from NIH EY030998

Talk 4, 3:15 pm, 54.14

Visual landmark information is multiplexed with target information in the visual responses of prefrontal gaze centres.

Vishal Bharmauria¹ (), Adrian Schütz², Xiaogang Yan¹, Hongying Wang¹, Frank Bremmer², John Douglas Crawford¹; ¹Centre for Vision Research (CVR) and Vision: Science to Applications (VISTA), York University, ²Department of Neurophysics, Phillips Universität Marburg and Center for Mind, Brain and Behavior – CMBB, Philipps-Universität Marburg and Justus-Liebig-Universität Giessen

How does the visual system extract useful information from a rich environment for action? For example, while reaching for a coffee cup, the brain may use several allocentric visual cues (nearby book or computer) to effectively grasp it. These landmarks influence spatial cognition and goal-directed behavior, but how landmark-related visual coding subserves action is poorly understood. To this goal, with gaze system as a model, we recorded 101/312 frontal (FEF) and 43/256 supplementary (SEF) eye field visual responses (in two head-unrestrained monkeys) to the presentation of a target (T, 100 ms), in presence of a visual landmark (L, intersecting lines; presented in one of four diagonal directions/configurations from T). First, using a response field model fitting approach, we confirmed our previous findings (Bharmauria et al. 2020, 2021) that Te (Target relative to initial 3D eye orientation) was the best model for FEF and SEF visual responses at the population level, but some neurons (30% in FEF and 20% in SEF) preferentially coded for landmark. We then specifically tested two mathematical continua (of ten equal steps) to quantify the influence of L on visual response: 1) Target to landmark in eye coordinates (Te-Le) that directly tested the influence of L and Target-in-eye to Target-relative-to landmark (Te-TL) to test the multiplexed influence of T and L. Along both continua, we found a significant influence of the landmark relative to the shuffled control data in most neurons (suggesting both landmark coding and influence of landmark on target coding). Further, the same analysis on separate T-L configurations resulted in a significant shift toward landmark-centered target coding at the population level in FEF, suggesting an influence of landmark coding. These results show that visual landmark influences visual responses in the gaze system, potentially stabilizing future gaze in the presence of noisy 3D eye position signals.

Acknowledgements: Canadian Institutes for Health Research (CIHR); Vision: Science to Applications (VISTA) Program: Deutsche Forschungsgemeinschaft (DFG)

Talk 5, 3:30 pm, 54.15

One Preferred Retinal Locus to rule them all: A fine dissection of the PRL in space and time

Josselin Gautier^1,2 (), Norick R. Bowers^2,3, Martin S. Banks², Austin Roorda²; ¹CHNO des Quinze-Vingts, Inserm-DGOS CIC 1423, F-75012 Paris, ²Herbert Wertheim School of Optometry and Vision Science, University of California Berkeley, ³Justus-Liebig-Universität Gießen, Germany

The preferred retinal locus (PRL) is defined functionally as the retinal position used to see or guide gaze. A refined definition of the PRL satisfying either the best performance (acuity) or stability (motor) will help inform about human foveal vision. A high-speed, sub-arcmin, retinal-image-based eye-tracker (Adaptive Optics Scanning Laser Ophthalmoscope:AOSLO) was used to measure PRL properties for a cadenced, fine-discrimination task. The AOSLO projects and unambiguously records the stimulus location over the constantly moving retinal image. Six subjects reported offsets between two tiny 2x1 arcmin horizontal Vernier bars separated by 1 arcmin along 7 offsets of 6 arcsecs. The bars were decrements presented within a 0.9° red AOSLO 30 frame-per-second display containing four fixation guides. Stimuli were flashed for two frames every 2sec in a cadence, so subjects could adopt a constant fixation strategy. 2100 trials were presented in pseudorandom order for each participant. Spatially-defined PRLs and fixation stabilities (ISOA) were computed for either all fixation points (PRL), fixation points during stimulus onset, saccade starting positions, saccade landing positions and the subset of positions leading to correct responses for the smallest Vernier offset (cPRL). Temporally defined PRLs were isolated at mid-drift duration between saccades or by the stable eye position plateau observed 200-400ms after stimulus onset (itPRL). Saccade rate, amplitude and landing distance to cPRL, corresponding fixation stability all work to reduce and converge 200-400ms after Vernier appearance. Interestingly this most stable, congruent epoch appears driven by finely programmed saccades in timing and landing position. Accurate image placement on the retina in both space and time is important for fine visual tasks. The observation of fixation ISOA decreasing after the brief stimulus may indicate a strategy to integrate visual information from normally more stationary targets. Overall, cPRL and itPRL offer the most reliable and meaningful functional definitions of the PRL.

Acknowledgements: R01EY023591, T32 EY007043

Talk 6, 3:45 pm, 54.16

Sinusoidal Smooth Pursuit After Childhood Hemispherectomy

Maria Z. Chroneos^1,2 (), Shawn M. Willet², Sophia Robert¹, J. Patrick Mayo², Marlene Behrmann^2,1; ¹Carnegie Mellon University, ²University of Pittsburgh

Smooth pursuit eye movements are crucial for tracking moving visual stimuli. This capacity is subserved by a bilateral network of brain regions including the frontal eye fields, basal ganglia, and occipitotemporal cortex (Sharpe, 2008, Lencer et al., 2008). Previous studies have demonstrated deficits in which adults with unilateral frontal or posterior lesions, or hemispherectomy execute saccades rather than smooth pursuit ipsilesionally (Morrow et al., 1995, Thurston et al., 1988, Troost et al., 1972). It is not known to what extent the smooth pursuit system is affected in those with childhood hemispherectomy for the treatment of drug-resistant epilepsy. We recorded eye movements using an EyeLink 1000 Plus during sinusoidal smooth pursuit in individuals with childhood hemispherectomy (n = 14, 10 left [LH] and 4 right [RH] hemispherectomies, age at surgery: < 1 month-8 years, age at test: 12-32 years). Participants tracked a target moving in a horizontal sinusoidal pattern (frequency = 0.3 Hz, amplitude = 10 degrees) for 4-12, 10 second trials. Qualitative visual analysis of sinusoidal trace plots shows that the participants generally followed the target, but had large variability in smooth pursuit, with many exhibiting frequent saccades, blinks, or other positional deviance from target position. To investigate possible asymmetries in this atypical pattern, we compared pursuit movements in the ipsilesional and contralesional direction for each participant. Every participant showed statistically significant differences between ipsilesional and contralesional movement variance (p < 0.05). To test whether these asymmetries can be explained by saccadic interruption of smooth pursuit, we computed the number of saccades during ipsilesional and contralesional movement from smoothed eye velocity traces. All 10 LH and one RH participant exhibited more ipsilesional than contralesional saccades. Surprisingly, the remaining RH participants did not show this atypical pattern. Overall, our results elucidate smooth pursuit asymmetries in individuals with childhood hemispherectomy.

Acknowledgements: NIH grant to MB (R01EY027018); MB acknowledges support from P30 CORE award EY08098 from the National Eye Institute, NIH, and unrestricted supporting funds from The Research to Prevent Blindness Inc, NY, and the Eye & Ear Foundation of Pittsburgh

Talk 7, 4:00 pm, 54.17

The eyes as a window to internal fluctuations in global brain state

Richard Johnston^1,2,3 (), Matthew A. Smith^1,2,3; ¹Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, USA, ²Carnegie Mellon Neuroscience Institute, Carnegie Mellon University, Pittsburgh, USA, ³Center for the Neural Basis of Cognition, Carnegie Mellon University, Pittsburgh, USA

On a daily basis, we perform a variety of perceptual tasks that depend on the precise encoding of sensory information. Our performance on these tasks is modulated by the internal state of the brain with respect to ongoing fluctuations in arousal, motivation and effort. Several studies have shown that signals related to these processes are embedded in the population activity of cortical neurons. For example, recent work identified a pattern of neural activity (termed "slow drift") in macaque visual and prefrontal cortex that is correlated with: 1) performance on a range of behavioral tasks; and 2) metrics related to the action of the eyes e.g., pupil size, microsaccade rate and saccade velocity. This motivated us to ask if slow drift is present in subcortical regions that have been implicated in oculomotor control. To this end, we recorded from populations of neurons in the superior colliculus (SC) and prefrontal cortex (PFC) of two monkeys while they performed a memory-guided saccade task. Using dimensionality reduction, we identified a pattern of neural activity in the SC that was strongly correlated with slow drift in the PFC. Furthermore, we found that slow drift in the SC was associated with a constellation of eye metrics including pupil size, microsaccade rate and saccade velocity. These findings are important for at least two reasons. Firstly, they highlight the brain-wide nature of fluctuations in arousal and demonstrate their presence in subcortical regions linked to gaze control. Secondly, they support a growing body of research suggesting that the action of the eyes, both when they move and during periods of steady fixation, can provide a window to internal states of the brain.