Hierarchical Gradients of Encoded Spatial and Sensory Information in the Neocortex Are Attenuated by Dorsal Hippocampal Lesions.

During navigation, the neocortex actively integrates learned spatial context with current sensory experience to guide behaviors. However, the relative encoding of spatial and sensorimotor information among cortical cells, and whether hippocampal feedback continues to modify these properties after learning, remains poorly understood. Thus, two-photon microscopy of male and female Thy1-GCaMP6s mice was used to longitudinally image neurons spanning superficial retrosplenial cortex and layers II-Va of primary and secondary motor cortices before and after bilateral dorsal hippocampal lesions. During behavior on a familiar cued treadmill, the locations of two obstacles were interchanged to decouple place-tuning from cue-tuning among position-correlated cells with fields at those locations. Subpopulations of place and cue cells each formed interareal gradients such that higher-level cortical regions exhibited higher fractions of place cells, whereas lower-level regions exhibited higher fractions of cue cells. Position-correlated cells in the motor cortex also formed translaminar gradients; more superficial cells were more likely to exhibit fields and were more sparsely and precisely tuned than deeper cells. After dorsal hippocampal lesions, a neural representation of the learned environment persisted, but retrosplenial cortex exhibited significantly increased cue-tuning, and, in motor cortices, both position-correlated cell recruitment and population activity at the unstable obstacle locations became more homogeneously elevated across laminae. Altogether, these results support that the hippocampus continues to modulate cortical responses in familiar environments, and the relative impact of descending feedback obeys hierarchical interareal and interlaminar gradients opposite to the flow of ascending sensory inputs.

Relative precision of top-down attentional modulations is lower in early visual cortex compared to mid- and high-level visual areas.

Top-down spatial attention enhances cortical representations of behaviorally relevant visual information and increases the precision of perceptual reports. However, little is known about the relative precision of top-down attentional modulations in different visual areas, especially compared with the highly precise stimulus-driven responses that are observed in early visual cortex. For example, the precision of attentional modulations in early visual areas may be limited by the relatively coarse spatial selectivity and the anatomical connectivity of the areas in prefrontal cortex that generate and relay the top-down signals. Here, we used functional MRI (fMRI) and human participants to assess the precision of bottom-up spatial representations evoked by high-contrast stimuli across the visual hierarchy. Then, we examined the relative precision of top-down attentional modulations in the absence of spatially specific bottom-up drive. Whereas V1 showed the largest relative difference between the precision of top-down attentional modulations and the precision of bottom-up modulations, midlevel areas such as V4 showed relatively smaller differences between the precision of top-down and bottom-up modulations. Overall, this interaction between visual areas (e.g., V1 vs. V4) and the relative precision of top-down and bottom-up modulations suggests that the precision of top-down attentional modulations is limited by the representational fidelity of areas that generate and relay top-down feedback signals.NEW & NOTEWORTHY When the relative precision of purely top-down and bottom-up signals were compared across visual areas, early visual areas like V1 showed higher bottom-up precision compared with top-down precision. In contrast, midlevel areas showed similar levels of top-down and bottom-up precision. This result suggests that the precision of top-down attentional modulations may be limited by the relatively coarse spatial selectivity and the anatomical connectivity of the areas generating and relaying the signals.

Top-Down Feedback Controls the Cortical Representation of Illusory Contours in Mouse Primary Visual Cortex.

Visual systems have evolved to recognize and extract features from complex scenes using limited sensory information. Contour perception is essential to this process and can occur despite breaks in the continuity of neighboring features. Such robustness of the animal visual system to degraded or occluded shapes may also give rise to an interesting phenomenon of optical illusions. These illusions provide a great opportunity to decipher neural computations underlying contour integration and object detection. Kanizsa illusory contours have been shown to evoke responses in the early visual cortex despite the lack of direct receptive field activation. Recurrent processing between visual areas has been proposed to be involved in this process. However, it is unclear whether higher visual areas directly contribute to the generation of illusory responses in the early visual cortex. Using behavior, in vivo electrophysiology, and optogenetics, we first show that the primary visual cortex (V1) of male mice responds to Kanizsa illusory contours. Responses to Kanizsa illusions emerge later than the responses to the contrast-defined real contours in V1. Second, we demonstrate that illusory responses are orientation-selective. Finally, we show that top-down feedback controls the neural correlates of illusory contour perception in V1. Our results suggest that higher-order visual areas may fill in the missing information in the early visual cortex necessary for illusory contour perception.SIGNIFICANCE STATEMENT Perception of the Kanizsa illusory contours is impaired in neurodevelopmental disorders such as schizophrenia, autism, and Williams syndrome. However, the mechanism of the illusory contour perception is poorly understood. Here we describe the behavioral and neural correlates of Kanizsa illusory contours perception in mice, a genetically tractable model system. We show that top-down feedback controls the neural responses to Kanizsa illusion in V1. To our knowledge, this is the first description of the neural correlates of the Kanizsa illusion in mice and the first causal demonstration of their regulation by top-down feedback.

Reversed Depth in Anticorrelated Random-Dot Stereograms and the Central-Peripheral Difference in Visual Inference.

In a random-dot stereogram, the percept of object surfaces in a three-dimensional scene is generated by images presented to left and right eyes that comprise interocularly corresponding random black and white dots. The spatial disparities between the corresponding dots determine the depths of object surfaces. If the dots are anticorrelated, such that a black dot in one monocular image corresponds to a white dot in the other, disparity-tuned neurons in the primary visual cortex (V1) respond as if their preferred disparities become nonpreferred and vice versa, thereby reversing the disparity signs reported to higher visual areas. Typically, when viewing anticorrelated random-dot stereograms presented in the central visual field, humans have great difficulty perceiving the reversed depth or indeed any coherent depth at all. We report that the reversed depth is more easily perceived in the peripheral visual field, supporting a recently proposed central-peripheral dichotomy in the way that feedback from higher to lower visual cortical areas implements visual inference.

Body-scaled perception is subjected to adaptation when repetitively judging opportunities for grasping.

Experimental evidence is given that the perceptual system adapts to repetitive task execution in a perceptual two-choice judgment task. Participants were tested with respect to their perception of opportunities for plank grasping. Participants had to report whether planks were perceived as objects being graspable with either one hand or two hands. When the plank size was gradually increased and subsequently decreased, transitions from one hand judgments to two hands judgments and vice versa were observed. Analysis of the transition scores revealed that the perceptual judgments were body-scaled, as it is known in the literature. However, judgments were also found to be context dependent. Judgment transition scores were affected in a systematic way by the kind of and the number of previously made judgments. The latter quantitative impact was observed in three related experiments and suggests that perceptual judgments about opportunities for action adapt to task repetition. Overall, the experimental findings are consistent with the predictions of a dynamical systems model, which assumes that perceptual judgments are emergent properties of a self-organizing process that involves inhibitory top-down feedback.

Rapid color categorization revealed by frequency-tagging-based EEG.

There has been much debate on whether color categories affect how we perceive color. Recent theories have put emphasis on the role of top-down influence on color perception that the original continuous color space in the visual cortex may be transformed into categorical encoding due to top-down modulation. To test the influence of color categories on color perception, we adopted an RSVP paradigm, where color stimuli were presented at a fast speed of 100 ms per stimulus and were forward and backward masked by the preceding and following stimuli. Moreover, no explicit color naming or categorization was required. In theory, backward masking with such a short interval in a passive viewing task should constrain top-down influence from higher-level brain areas. To measure any potentially subtle differences in brain response elicited by different color categories, we embedded a sensitive frequency-tagging-based EEG paradigm within the RSVP stimuli stream where the oddball color stimuli were encoded with a different frequency from the base color stimuli. We showed that EEG responses to cross-category oddball colors at the frequency where the oddball stimuli were presented was significantly larger than the responses to within-category oddball colors. Our study suggested that the visual cortex can automatically and implicitly encode color categories when color stimuli are presented rapidly.

A neural model of modified excitation/inhibition and feedback levels in schizophrenia.

Introduction: The strength of certain visual illusions, including contrast-contrast and apparent motion, is weakened in individuals with schizophrenia. Such phenomena have been interpreted as the impaired integration of inhibitory and excitatory neural responses, and impaired top-down feedback mechanisms. Methods: To investigate whether and how these factors influence the perceived contrast-contrast and apparent motion illusions in individuals with schizophrenia, we propose a two-layer network, with top-down feedback from layer 2 to layer 1 that can model visual receptive fields (RFs) and their inhibitory and excitatory subfields. Results: Our neural model suggests that illusion perception changes in individuals with schizophrenia can be influenced by altered top-down mechanisms and the organization of the on-center off-surround receptive fields. Alteration of the RF inhibitory surround and/or the excitatory center can replicate the difference of illusion precepts between individuals with schizophrenia within certain clinical states and normal controls. The results show that the simulated top-down feedback modulation enlarges the difference of the model illusion representations, replicating the difference between the two groups. Discussion: We propose that the heterogeneity of visual and in general sensory processing in certain clinical states of schizophrenia can be largely explained by the degree of top-down feedback reduction, emphasizing the critical role of top-down feedback in illusion perception, and to a lesser extent on the imbalance of excitation/inhibition. Our neural model provides a mechanistic explanation for the modulated visual percepts of contrast-contrast and apparent motion in schizophrenia with findings that can explain a broad range of visual perceptual observations in previous studies. The two-layer motif of the current model provides a general framework that can be tailored to investigate subcortico-cortical (such as thalamocortical) and cortico-cortical networks, bridging neurobiological changes in schizophrenia and perceptual processing.

A neural model of modified excitation/inhibition and feedback levels in schizophrenia.

The strength of certain visual illusions is weakened in individuals with schizophrenia. Such phenomena have been interpreted as the impaired integration of inhibitory and excitatory neural responses, and impaired top-down feedback mechanisms. To investigate whether and how these factors influence the perceived illusions in individuals with schizophrenia, we propose a two-layer network that can model visual receptive fields (RFs), their inhibitory and excitatory subfields, and the top-down feedback. Our neural model suggests that illusion perception changes in individuals with schizophrenia can be influenced by altered top-down mechanisms and the organization of the on-center off-surround receptive fields. Alteration of the RF inhibitory surround and/or the excitatory center can replicate the difference of illusion precepts between individuals with schizophrenia and normal controls. The results show that the simulated top-down feedback modulation enlarges the difference of the model illusion representations, replicating the difference between the two groups. We propose that the heterogeneity of visual and in general sensory processing in schizophrenia can be largely explained by the degree of top-down feedback reduction, emphasizing the critical role of top-down feedback in illusion perception, and to a lesser extent on the imbalance of excitation/inhibition. Our neural model provides a mechanistic explanation for the modulated visual percepts in schizophrenia with findings that can explain a broad range of visual perceptual observations in previous studies. The two-layer motif of the current model provides a general framework that can be tailored to investigate subcortico-cortical (such as thalamocortical) and cortico-cortical networks, bridging neurobiological changes in schizophrenia and perceptual processing.

Central-peripheral dichotomy: color-motion and luminance-motion binding show stronger top-down feedback in central vision.

Recently a theory (Zhaoping, Vision Research, 136, 32-49, 2017) proposed that top-down feedback from higher to lower visual cortical areas, to aid visual recognition, is stronger in the central than in the peripheral visual fields. Since top-down feedback helps feature binding, a critical visual recognition process, this theory predicts that insufficient feedback in the periphery should make feature misbinding more likely. To test this prediction, this study assessed binding between color and motion features, or between luminance and motion features, at different visual field eccentricities. We first used color-motion stimuli containing equiluminant red and green dots moving in opposite directions, for example, red dots moved leftward while green dots moved rightward. Such stimuli were shown in both a central reference strip and a peripheral test strip; participants reported whether it was the first or second interval in a trial in which the dots of each color moved in the opposite directions between the two strips. The center of the test strip was at 4° or 15° away from the gaze fixation. Participants' performance was much worse when the test strip was more peripheral, suggesting that feature misbinding occurred more frequently there. This held even when the size and density of the dots were adjusted by eccentricity-dependent cortical magnification factors, and even when red/green dots were replaced by yellow/blue dots or black/white dots to suit the retinal input sampling peripherally. Our findings support that top-down feedback is more directed to central vision, which can resolve ambiguities in feature binding at more central visual locations.

Contrast-reversed binocular dot-pairs in random-dot stereograms for depth perception in central visual field: Probing the dynamics of feedforward-feedback processes in visual inference.

In a random-dot stereogram (RDS), the spatial disparities between the interocularly corresponding black and white random dots determine the depths of object surfaces. If a black dot in one monocular image corresponds to a white dot in the other, disparity-tuned neurons in primary visual cortex (V1) respond as if their preferred disparities become non-preferred and vice versa, reversing the disparity sign reported to higher visual areas. Reversed depth is perceptible in the peripheral but not the central visual field. This study demonstrates that, in central vision, adding contrast-reversed dots to a noisy RDS (containing the normal contrast-matched dots) can augment or degrade depth perception. Augmentation occurs when the reversed depth signals are congruent with the normal depth signals to report the same disparity sign, and occurs regardless of the viewing duration. Degradation occurs when the reversed and normal depth signals are incongruent with each other and when the RDS is viewed briefly. These phenomena reflect the Feedforward-Feedback-Verify-and-reWeight (FFVW) process for visual inference in central vision, and are consistent with the central-peripheral dichotomy that central vision has a stronger top-down feedback from higher to lower brain areas to disambiguate noisy and ambiguous inputs from V1. When a RDS is viewed too briefly for feedback, augmentation and degradation work by adding the reversed depth signals from contrast-reversed dots to the feedforward, normal, depth signals. With a sufficiently long viewing duration, the feedback vetoes incongruent reversed depth signals and amends or completes the imperfect, but congruent, reversed depth signals by analysis-by-synthesis computation.

The Flip Tilt Illusion: Visible in Peripheral Vision as Predicted by the Central-Peripheral Dichotomy.

Consider a gray field comprising pairs of vertically aligned dots; in each pair, one dot is white the other black. When viewed in a peripheral visual field, these pairs appear horizontally aligned. By the Central-Peripheral Dichotomy, this flip tilt illusion arises because top-down feedback from higher to lower visual cortical areas is too weak or absent in the periphery to veto confounded feedforward signals from the primary visual cortex (V1). The white and black dots in each pair activate, respectively, on and off subfields of V1 neural receptive fields. However, the sub-fields' orientations, and the preferred orientations, of the most activated neurons are orthogonal to the dot alignment. Hence, V1 reports the flip tilt to higher visual areas. Top-down feedback vetoes such misleading reports, but only in the central visual field.

A Neural-Dynamic Architecture for Concurrent Estimation of Object Pose and Identity.

Handling objects or interacting with a human user about objects on a shared tabletop requires that objects be identified after learning from a small number of views and that object pose be estimated. We present a neurally inspired architecture that learns object instances by storing features extracted from a single view of each object. Input features are color and edge histograms from a localized area that is updated during processing. The system finds the best-matching view for the object in a novel input image while concurrently estimating the object's pose, aligning the learned view with current input. The system is based on neural dynamics, computationally operating in real time, and can handle dynamic scenes directly off live video input. In a scenario with 30 everyday objects, the system achieves recognition rates of 87.2% from a single training view for each object, while also estimating pose quite precisely. We further demonstrate that the system can track moving objects, and that it can segment the visual array, selecting and recognizing one object while suppressing input from another known object in the immediate vicinity. Evaluation on the COIL-100 dataset, in which objects are depicted from different viewing angles, revealed recognition rates of 91.1% on the first 30 objects, each learned from four training views.

Feedback from higher to lower visual areas for visual recognition may be weaker in the periphery: Glimpses from the perception of brief dichoptic stimuli.

Eye movements bring attended visual inputs to the center of vision for further processing. Thus, central and peripheral vision should have different functional roles. Here, we use observations of visual perception under dichoptic stimuli to infer that there is a difference in the top-down feedback from higher brain centers to primary visual cortex. Visual stimuli to the two eyes were designed such that the sum and difference of the binocular input from the two eyes have the form of two different gratings. These gratings differed in their motion direction, tilt direction, or color, and duly evoked ambiguous percepts for the corresponding feature. Observers were more likely to perceive the feature in the binocular summation rather than the difference channel. However, this perceptual bias towards the binocular summation signal was weaker or absent in peripheral vision, even when central and peripheral vision showed no difference in contrast sensitivity to the binocular summation signal relative to that to the binocular difference signal. We propose that this bias can arise from top-down feedback as part of an analysis-by-synthesis computation. The feedback is of the input predicted using prior information by the upper level perceptual hypothesis about the visual scene; the hypothesis is verified by comparing the feedback with the actual visual input. We illustrate this process using a conceptual circuit model. In this framework, a bias towards binocular summation can arise from the prior knowledge that inputs are usually correlated between the two eyes. Accordingly, a weaker bias in the periphery implies that the top-down feedback is weaker there. Testable experimental predictions are presented and discussed.

Goal-directed control with cortical units that are gated by both top-down feedback and oscillatory coherence.

The brain is able to flexibly select behaviors that adapt to both its environment and its present goals. This cognitive control is understood to occur within the hierarchy of the cortex and relies strongly on the prefrontal and premotor cortices, which sit at the top of this hierarchy. Pyramidal neurons, the principal neurons in the cortex, have been observed to exhibit much stronger responses when they receive inputs at their soma/basal dendrites that are coincident with inputs at their apical dendrites. This corresponds to inputs from both lower-order regions (feedforward) and higher-order regions (feedback), respectively. In addition to this, coherence between oscillations, such as gamma oscillations, in different neuronal groups has been proposed to modulate and route communication in the brain. In this paper, we develop a simple, but novel, neural mass model in which cortical units (or ensembles) exhibit gamma oscillations when they receive coherent oscillatory inputs from both feedforward and feedback connections. By forming these units into circuits that can perform logic operations, we identify the different ways in which operations can be initiated and manipulated by top-down feedback. We demonstrate that more sophisticated and flexible top-down control is possible when the gain of units is modulated by not only top-down feedback but by coherence between the activities of the oscillating units. With these types of units, it is possible to not only add units to, or remove units from, a higher-level unit's logic operation using top-down feedback, but also to modify the type of role that a unit plays in the operation. Finally, we explore how different network properties affect top-down control and processing in large networks. Based on this, we make predictions about the likely connectivities between certain brain regions that have been experimentally observed to be involved in goal-directed behavior and top-down attention.