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Nienborg, H.

Publications and source records attributed to Nienborg, H..

10 recordsLinked to original sources

Decoupling Choice from Motor Response Reduces Choice-History Effects

Perception and action form a loop as an organism interacts with its environment. Here, we probe the interdependence between the two in the context of choice-history effects, the tendency of past choices and their outcomes to bias current choices. We investigated if the modulation by previous choices depended on the coupling between perceptual choices and the motor responses reporting these choices. We analyzed data from non-human primates (Macaca mulatta; three females and five males) performing two different perceptual decision-making tasks. Each task had a "coupled" variant with a fixed mapping between perceptual choices and motor plans used to report the choice, and an "uncoupled" variant, in which this mapping varied randomly across trials. We found that, in both tasks, the animals in the coupled variant had larger choice-history effects compared to the animals in the uncoupled variant. Decoupling choices from motor responses was further associated with an inability by the animals to learn experimentally induced stimulus sequence regularities. Together, these findings identify choice-response coupling as a factor shaping animals ability to use recent history to guide behavior and highlight the tight link between cognitive and motor processes.

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Reassessing Choice Probability: What 59 Macaque Studies Tell Us About Decision-Related Activity in Visual Cortex

Choice probability (CP) quantifies the trial-by-trial covariation between a sensory neurons response and perceptual reports. Despite extensive interest in CP as a window into how perception is linked to the activity of sensory neurons, the usefulness of CP remains debated. On one hand, reported CP magnitudes vary widely across seemingly equivalent studies, questioning its utility as a metric. On the other hand, the absence of clear patterns in CP variability has made it difficult to use it to adjudicate between competing models of visual perception. Here, we performed a meta-analysis of 150 CP estimates from 59 macaque neurophysiology studies to identify factors that systematically influence CP. We confirmed the positive relationship between CP and neuronal sensitivity both across and within individual studies. When controlled for sensitivity, we found remarkable consistency in CP across varying tasks and brain regions with two notable exceptions. First, CPs were higher in tasks involving bistable percepts, reinforcing the link between CP magnitude and subjective perception. Second, CPs were smaller in area V1, supporting prior suggestions about V1s special role in visual processing. We further found a significant effect of stimulus duration on CP, providing evidence against strictly feedforward models and favoring models with substantial feedback and recurrent processing. Finally, we offer recommendations for future studies to enhance the cross-study comparability and theoretical utility of choice signals as the field transitions to large-scale population recordings. More broadly, our findings demonstrate the benefits of meta-studies that expose patterns across many different tasks and animals - yielding insights that complement large-scale population recordings.

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Retrograde Optogenetics Reveals Functional Convergence within a Corticotectal Pathway of Non-Human Primates

Understanding how the cerebral cortex communicates with subcortical areas to drive behavior remains a central question in system neuroscience. One key unresolved issue is whether prefrontal cortical outputs to motor-related subcortical regions carry predominantly motor commands or mixed sensory-motor signals. Retrograde optogenetics offers a powerful way to interrogate such projection-defined circuits, but its use in non-human primates has been limited. Here, we applied retrograde optogenetics in awake macaques to directly test the functional organization of the corticotectal projection from the frontal eye field (FEF) to the superior colliculus (SC). We asked whether the FEF output signals to SC are motor-dominant or broadly sensory-motor. Optical activation of this pathway evoked robust, contralateral saccades and selectively modulated reaction times, demonstrating its causal role in saccade generation. Optogenetically tagging FEF neurons projecting to SC revealed a heterogeneous population of visual, visuomotor, and motor neurons. This diverse output converged predominantly onto motor-related neurons in the SC. These findings support a visuomotor convergence model, in which diverse FEF outputs drive motor-selective SC neurons with activity sufficient for saccade generation, and thus resolve long-standing questions over the composition of FEF outputs. Additionally, our results establish retrograde optogenetics as a tool for dissecting projection-defined circuits in primates and for precisely probing the neural pathways that link perception to action. HighlightsRetrograde optogenetics enabled pronounced and selective modulation of behavior in macaques. Selective optical stimulation of the FEF-SC pathway evoked contralateral saccades and modulated reaction times. Opto-tagging revealed diverse visual, visuomotor, and motor FEF outputs converging onto motor-related SC neurons. Findings support a visuomotor convergence model and demonstrate the power of projection-specific optogenetic tools in primates.

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Activity in primate visual cortex is minimally driven by spontaneous movements

Organisms process sensory information in the context of their own moving bodies, an idea referred to as embodiment. This idea is important for developmental neuroscience, and increasingly plays a role in robotics and systems neuroscience. The mechanisms that support such embodiment are unknown, but a manifestation could be the observation in mice of brain-wide neuromodulation, including in the primary visual cortex, driven by task-irrelevant spontaneous body movements. Here we tested this hypothesis in macaque monkeys, a primate model for human vision, by simultaneously recording visual cortex activity and facial and body movements. Activity in the visual cortex (V1, V2, V3/V3A) was associated with the animals own movements, but this modulation was largely explained by the impact of the movements on the retinal image. These results suggest that embodiment in primate vision may be realized by input provided by the eyes themselves.

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Binocular disparity-based learning does not generalize to the other visual hemifield

Visual perceptual learning refers to long-lasting performance improvements on a visual skill, an ability presumably supported by plastic changes in early visual brain areas. Visual perceptual learning has been shown to be induced by training and to benefit from consolidation during sleep, presumably via the reactivation of learning-associated neuronal firing patterns. However, previous studies have almost exclusively relied on a single paradigm, the texture discrimination task, on which performance improvements may not rely on strictly perceptual skills. Here, we tested whether sleep has beneficial effects on a visual disparity discrimination task. We confirm previous findings in showing that the ability to discriminate different disparities is unaffected by sleep during a 12-hour retention period after training. Importantly, we extend these results by providing evidence against an effect of sleep on the generalization of improved disparity discrimination across the vertical meridian. We further rule out carry-over effects as a possible confound in our earlier within-subject study by relying on a between-subject design. The combined data from both studies argue against sleep as an important factor in the consolidation of a strictly perceptual skill. This sets important constraints on models of the role of sleep and sleep-associated neural reactivation in the consolidation of non-declarative memories.

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Easily adaptable head-free training system of macaques for tasks requiring precise measurements of eye position

We describe a modified system for training macaque monkeys without invasive head immobilization on visuomotor tasks requiring the control of eye-movements. The system combines a conventional primate chair, a chair-mounted infrared camera for measuring eye-movements and a custom-made concave reward-delivery spout firmly attached to the chair. The animal was seated head-free inside the chair but the concavity of the spout stabilized its head during task performance. Training on visual fixation and discrimination tasks was successfully performed with this system. Eye-measurements, such as fixation-precision, pupil size as well as micro-saccades were comparable to those obtained using conventional invasive head-fixation methods. The system is inexpensive ([~]$40 USD material cost), easy to fabricate in a workshop (technical drawings are included), and readily adjustable between animals without the need to immobilize or sedate them for these adjustments.\n\nHighlightsO_LIWe developed an approach to train macaque monkeys head-free on visuomotor tasks requiring measurements of eye position\nC_LIO_LIThe setup is inexpensive, easy to build, and readily adjusted to the animal without the need for sedation\nC_LIO_LIThe system was tested for training on a visual fixation and a visual discrimination task\nC_LIO_LIEye measurements (fixation precision, pupil size, microsaccades) were comparable to those from head-fixed animals\nC_LI

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Manipulating patterns of dynamic deformation elicits the impression of cloth with varying stiffness

Cloth is a common material and humans can visually estimate its mechanical properties by observing how it deforms under external forces. Here we ask whether, and how, dynamic deformation can affect the perception of mechanical properties of cloth. In Experiment 1, we find that both intrinsic mechanical properties and optical properties affect stiffness perception when the stimuli are presented as images. By contrast, in videos, humans can partially discount the effect of optical appearances and exhibit higher sensitivity to stiffness. We further identified an idiosyncratic deformation pattern (i.e., movement uniformity) to differentiate stiffness, which can be reliably measured by six optical flow features. In Experiment 2, we isolate the deformation by creating dynamic dot stimuli from the 3D mesh of the cloth. We directly alter the movement pattern by manipulating the uniformity of the displacement vectors on the dot stimuli, and show that changing the pattern of dynamic deformation alone can alter the perceived stiffness of cloth in a variety of scene set-ups. Furthermore, by analyzing optical flow fields extracted from the manipulated dynamic dot stimuli, we confirmed the same six optical flow features can be diagnostic of the degree of stiffness of moving cloth across different scenes. Overall, our study demonstrates that manipulating patterns of dynamic deformation alone can elicit the impression of cloth with varying stiffness, suggesting that human visual system might rely on the idiosyncratic pattern of dynamic deformation for estimating stiffness.

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Human-level saccade detection performance using deep neural networks

Saccades are ballistic eye movements that rapidly shift gaze from one location of visual space to another. Detecting saccades in eye movement recordings is important not only for studying the neural mechanisms underlying sensory, motor, and cognitive processes, but also as a clinical and diagnostic tool. However, automatically detecting saccades can be difficult, particularly when such saccades are generated in coordination with other tracking eye movements, like smooth pursuits, or when the saccade amplitude is close to eye tracker noise levels, like with microsaccades. In such cases, labeling by human experts is required, but this is a tedious task prone to variability and error. We developed a convolutional neural network (CNN) to automatically detect saccades at human-level performance accuracy. Our algorithm surpasses state of the art according to common performance metrics, and will facilitate studies of neurophysiological processes underlying saccade generation and visual processing.

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Estimating mechanical properties of cloth from videos using dense motion trajectories: human psychophysics and machine learning

Humans can visually estimate the mechanical properties of deformable objects (e.g. cloth stiffness). While much of the recent work on material perception has focused on static image cues (e.g., textures and shape), little is known whether humans can integrate information over time to make a judgment. Here, we investigate the effect of spatiotemporal information across multiple frames (multi-frame motion) on estimating the bending stiffness of cloth. Using high-fidelity cloth animations, we first examined how the perceived bending stiffness changed as a function of the physical bending stiffness defined in the simulation model. Using maximum likelihood difference scaling methods (MLDS) we found that the perceived stiffness and the physical bending stiffness were highly correlated. A second experiment in which we scrambled the frame sequences diminished this correlation. This suggests that multi-frame motion plays an important role. To provide further evidence for this finding, we extracted dense motion trajectories from the videos across 15 consecutive frames and used the trajectory descriptors to train a machine-learning model with the measured perceptual scales. The model can predict human perceptual scales in new videos with varied winds, optical properties of cloth, and scene setups. When the correct multi-frame was removed (using either scrambled videos or 2-frame optical flow to train the model), the predictions significantly worsened. Our findings demonstrate that multi-frame motion information is important for both humans and machines to estimate the mechanical properties. In addition, we show that dense motion trajectories are effective features to build a successful automatic cloth estimation system.

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Using confidence inferred from pupil-size to dissect perceptual task-strategy: support for a bounded decision-formation process

During perceptual decisions subjects often rely more strongly on early rather than late sensory evidence even in tasks when both are equally informative about the correct decision. This early psychophysical weighting has been explained by an integration-to-bound decision process, in which the stimulus is ignored after the accumulated evidence reaches a certain bound, or confidence level. Here, we derive predictions about how the average temporal weighting of the evidence depends on a subjects decision-confidence in this model. To test these predictions empirically, we devised a method to infer decision-confidence from pupil size in monkeys performing a disparity discrimination task. Our animals data confirmed the integration-to-bound predictions, with different internal decision-bounds accounting for differences between animals. However, the data could not be explained by two alternative accounts for early psychophysical weighting: attractor dynamics either within the decision area or due to feedback to sensory areas, or a feedforward account due to neuronal response adaptation. This approach also opens the door to using confidence more broadly when studying the neural basis of decision-making.

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