How we make saccades: selection, control, integration

Organizers: Emma Stewart1, Bianca R. Baltaretu1; 1Justus-Liebig University Giessen, Germany
Presenters: Jacqueline Gottlieb, Michele Basso, J. Patrick Mayo, J. Douglas Crawford, Alexander C. Schütz

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Everyday behaviour is facilitated by our ability to correctly locate and fixate pertinent objects and locations within our surroundings. This is accomplished through the 2-3 saccades per second that are made to gather visual information and guide actions. With each saccade, however, a complex series of processes occurs: a saccade target must be selected, motor commands must ensure accurate saccade execution, and the perceptual consequences of making a saccade need to be accounted for. Over the past few decades, a wealth of research has given us insight into the related, intricate neural and behavioural mechanisms underlying saccade production. However, recent research has uncovered more nuanced roles for key established neural regions associated with the selection, control, and integration of saccadic eye movements. These regions extend from subcortical superior colliculus (SC) to the frontal cortex (i.e., frontal eye field, FEF) and posterior parietal cortex (Sommer & Wurtz, 1998, 2004; Medendorp et al., 2003). New evidence has also been uncovered about the goals and strategies of saccade target selection, and about how saccades actively shape and change our predictions about, and perception of, the world. While the underlying circuitry may have been identified, there is a significant gap in our knowledge about the complex interactions between the discrete neural components of a saccade, the goals that drive saccades, and the perception of the world that precedes and follows these events. In this symposium, leading researchers will unveil a more sophisticated perspective on the sequence of processes that occur before, during, and after a saccade, in humans and non-human primates, with a focus on three key areas. 1) Selection: What complex neural and behavioral processes underlie target selection? What new evidence is there for where perceptual decisions that drive saccades occur in the brain? Jacqueline Gottlieb will outline the link between target selection and uncertainty reduction in belief states, linking theories of information sampling with neurophysiological evidence. Furthermore, Michele Basso will highlight a new role for the superior colliculus in perceptual decision-making, reforming our understanding of the function of this subcortical structure. 2) Control: Once a target is selected, how does the visuomotor system exert its control over eye movements? J. Patrick Mayo will discuss new neurophysiological findings on the crucial role that FEF neurons play in online oculomotor control and decisions. 3) Integration: How does the visual system reconcile behaviourally and cortically pre- and postsaccadic information to perceive a seamless world across saccades? Doug Crawford will reveal the nature and identity of the cortical mechanism(s) that underlie object feature integration across saccades, and for action (i.e., grasping). Finally, Alexander Schütz will discuss recent behavioural and computational insights into how humans reconcile the perceptual differences in peripheral and foveal input across saccades, which will outline how we ultimately perceive the world across saccades. By bringing together behavioural, neurophysiological, neuroimaging, and computational findings, this symposium will present groundbreaking new advances that will establish a contemporary understanding of how saccades are made.

Presentations

Saccadic control for reducing uncertainty

Jacqueline Gottlieb1; 1Columbia University

Saccades gather visual information. Although few scientists would question this statement, the neural mechanisms of saccade target selection are typically described in terms of reward with no reference to information. I will describe evidence from my laboratory that attentional sampling is sensitive to expected information gains (EIG). Saccade selective neurons in the parietal cortex are modulated by the two quantities that determine EIG - uncertainty and predictive validity - independently of rewards. Moreover, the effects of uncertainty before the saccade modulate the efficiency with which monkeys use the information after the saccade. The findings suggest that saccade target selection is closely coordinated with our belief states and is geared toward reducing the future uncertainty of those states.

A causal role of the primate superior colliculus in perceptual decision-making

Michele Basso1; 1University of California Los Angeles

People with Parkinson’s disease show impairments in their ability to use memory information to guide choices of action when faced with perceptual uncertainty. Changes in the inhibitory output of the basal ganglia underlies motor symptoms in Parkinson’s disease. The superior colliculus, a brainstem target of the basal ganglia, is known to play a role in aspects of attention and decision-making. Therefore, we asked whether changes in the level of inhibition in the superior colliculus altered the ability of monkeys to make perceptual decisions. Trained monkeys performed a two-choice perceptual decision-making task in which they reported the perceived orientation of a dynamic Glass pattern, before and after unilateral, reversible, inactivation of the superior colliculus. We found that unilateral SC inactivation produced significant decision biases and changes in reaction times consistent with a causal role for the primate superior colliculus in perceptual decision-making. Fitting signal detection theory and sequential sampling models to the data showed that superior colliculus inactivation produced a decrease in the relative evidence for contralateral decisions, as if adding a constant offset to a time-varying evidence signal for the ipsilateral choice. The results provide causal evidence for an embodied cognition model of perceptual decision-making and provide compelling evidence that the superior colliculus of primates (a brainstem structure) plays a causal role in how evidence is computed for decisions-a process usually attributed to the forebrain.

The interaction of saccadic and smooth pursuit eye movements signals in macaque frontal eye fields

J. Patrick Mayo1, Ruitong "Larry" Jiang1; 1The University of Pittsburgh

Natural vision involves the constant coordination of multiple different types of eye movements. Prior research has tended to focus on behavioral and neuronal correlates of a single type of eye movement (e.g., only saccades or only smooth pursuit). These investigations have set the stage for our current work on the selection and control of different types of eye movements. We recorded neuronal activity in the macaque frontal eye fields, a region of prefrontal cortex with an established role in saccadic control and smooth pursuit, while monkeys made saccades and pursuit in one of eight directions. Although the interaction of saccade and pursuit signals is traditionally thought to be minimal in FEF, we set out to test this idea by recording from populations of neurons using multi-contact linear electrode arrays. Taking inspiration from the classic characterization of visual-saccadic activity in FEF ("VMI"; visual-motor index), we created a contrast ratio called the Saccade Pursuit Index (SPI) to measure the relative firing rates of individual neurons to saccadic and smooth pursuit eye movements. We found that a large proportion of neurons elicited roughly equal firing rates during saccades and pursuit, forming a relatively continuous and unimodal distribution of SPI values. We extended our analyses to pairs of simultaneously recorded neurons, where the independence of saccadic and pursuit signals was evaluated using spike count correlations ("noise" correlations). Our results suggest that FEF neurons interact across different types of eye movements more than previously assumed, implicating FEF in the online control of real-time oculomotor decisions.

Cortical networks for transsaccadic perception: fMRI and functional connectivity

J. Douglas Crawford1, Bianca R. Baltaretu2, Benjamin T. Dunkley3, George Tomou1; 1York University, Toronto, Canada, 2Justus-Liebig University Giessen, Germany, 3Hospital for Sick Children, Toronto, Canada

Transsaccadic perception (TSP) requires the retention, updating, and integration / comparison of visual information obtained before and after a saccade. Based on our earlier psychophysical and TMS studies, we hypothesized that TSP taps into frontoparietal mechanisms for spatial updating, and that low level location/feature integration might occur through feedback to occipital cortex, whereas higher level interactions might occur through lateral dorsoventral connectivity or prefrontal convergence (e.g., Prime et al., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2011). Here, we set about localizing these interactions using an fMRI adaptation paradigm. We found evidence for transsaccadic orientation perception in supramarginal gyrus (SMG) (Dunkley et al., Cortex 2016). We then extended SMG’s role to updating object orientation for grasp, engaging a functional network including the frontal eye fields and parietal grasp areas (Balaretu et al., J. Neurosci. 2021). However, when we applied this approach to spatial frequency, we found saccade-feature interactions in dorsal occipital cortex (Baltaretu et al., Sci. Rep. 2021). Most recently, we employed a task involving transsaccadic discrimination of object orientation versus shape (Baltaretu et al., bioRxiv 2021). Graph theory analysis revealed a bilateral dorsal functional module extending across parietofrontal cortex, whereas saccade-feature interactions fell within two lateralized occipital modules that rejoined in the presence of saccades. Overall, our data are consistent with the notion that TSP is a cortical network phenomenon that includes interactions between saccade signals and spatial features (location, orientation) in parietal cortex versus identity-related features (spatial frequency, shape) in occipital cortex.

Interaction of peripheral and central visual information in transsaccadic perception

Alexander C. Schütz1, Emma E.M. Stewart2, Matteo Valsecchi3; 1Phillips-Universität Marburg, Germany, 2Justus-Liebig University Giessen, Germany, 3Universitá di Bologna, Italy

In active vision, relevant objects are selected in the peripheral visual field and then brought to the central visual field by saccadic eye movements. Hence, there are usually two sources of visual information about an object: information from peripheral vision before a saccade and information from central vision after a saccade. The well-known differences in processing and perception between the peripheral and the central visual field lead to the question whether and how the two pieces of information are matched and combined. This talk will provide an overview about different mechanisms that may alleviate differences between peripheral and central representations and allow for a seamless perception across saccades. Transsaccadic integration results in a weighted combination of peripheral and central information according to their relative reliability, such that uncertainty is minimized. It is a resource-limited process that does not apply to the whole visual field, but only to attended objects. Nevertheless, it is not strictly limited to the saccade target, but can be flexibly directed to other relevant locations. Transsaccadic prediction uses peripheral information to estimate the most likely appearance in the central visual field. This allows appearance to be calibrated in the peripheral and central visual field. Such a calibration is not only relevant to maintain perceptual stability across saccades, but also to match templates for visual search in peripheral and central vision.

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