How Does the Cerebral Cortex Work? Developement, Learning, Attention, and 3D Vision by Laminar Circuits of Visual Cortex

A key goal of behavioral and cognitive neuroscience is to link brain mechanisms to behavioral functions. The present article describes recent progress towards explaining how the visual cortex sees. Visual cortex, like many parts of perceptual and cognitive neocortex, is organized into six main layers of cells, as well as characteristic sub-lamina. Here it is proposed how these layered circuits help to realize the processes of developement, learning, perceptual grouping, attention, and 3D vision through a combination of bottom-up, horizontal, and top-down interactions. A key theme is that the mechanisms which enable developement and learning to occur in a stable way imply properties of adult behavior. These results thus begin to unify three fields: infant cortical developement, adult cortical neurophysiology and anatomy, and adult visual perception. The identified cortical mechanisms promise to generalize to explain how other perceptual and cognitive processes work.

Linking Visual Cortex to Visual Perception: An Alternative to the Gestalt Bubble

Lehar's lively discussion builds on a critique of neural models of vision that is incorrect in its general and specific claims. He espouses a Gestalt perceptual approach, rather than one consistent with the "objective neurophysiological state of the visual system" (p. 1). Contemporary vision models realize his perceptual goals and also quantitatively explain neurophysiological and anatomical data.

Temporal Dynamics of Decision-Making during Motion Perception in the Visual Cortex

How does the brain make decisions? Speed and accuracy of perceptual decisions covary with certainty in the input, and correlate with the rate of evidence accumulation in parietal and frontal cortical "decision neurons." A biophysically realistic model of interactions within and between Retina/LGN and cortical areas V1, MT, MST, and LIP, gated by basal ganglia, simulates dynamic properties of decision-making in response to ambiguous visual motion stimuli used by Newsome, Shadlen, and colleagues in their neurophysiological experiments. The model clarifies how brain circuits that solve the aperture problem interact with a recurrent competitive network with self-normalizing choice properties to carry out probablistic decisions in real time. Some scientists claim that perception and decision-making can be described using Bayesian inference or related general statistical ideas, that estimate the optimal interpretation of the stimulus given priors and likelihoods. However, such concepts do not propose the neocortical mechanisms that enable perception, and make decisions. The present model explains behavioral and neurophysiological decision-making data without an appeal to Bayesian concepts and, unlike other existing models of these data, generates perceptual representations and choice dynamics in response to the experimental visual stimuli. Quantitative model simulations include the time course of LIP neuronal dynamics, as well as behavioral accuracy and reaction time properties, during both correct and error trials at different levels of input ambiguity in both fixed duration and reaction time tasks. Model MT/MST interactions compute the global direction of random dot motion stimuli, while model LIP computes the stochastic perceptual decision that leads to a saccadic eye movement.

Spiking Dynamics during Perceptual Grouping in the Laminar Circuits of Visual Cortex

Grouping of collinear boundary contours is a fundamental process during visual perception. Illusory contour completion vividly illustrates how stable perceptual boundaries interpolate between pairs of contour inducers, but do not extrapolate from a single inducer. Neural models have simulated how perceptual grouping occurs in laminar visual cortical circuits. These models predicted the existence of grouping cells that obey a bipole property whereby grouping can occur inwardly between pairs or greater numbers of similarly oriented and co-axial inducers, but not outwardly from individual inducers. These models have not, however, incorporated spiking dynamics. Perceptual grouping is a challenge for spiking cells because its properties of collinear facilitation and analog sensitivity to inducer configurations occur despite irregularities in spike timing across all the interacting cells. Other models have demonstrated spiking dynamics in laminar neocortical circuits, but not how perceptual grouping occurs. The current model begins to unify these two modeling streams by implementing a laminar cortical network of spiking cells whose intracellular temporal dynamics interact with recurrent intercellular spiking interactions to quantitatively simulate data from neurophysiological experiments about perceptual grouping, the structure of non-classical visual receptive fields, and gamma oscillations.

Texture Segregation By Visual Cortex: Perceptual Grouping, Attention, and Learning

A neural model is proposed of how laminar interactions in the visual cortex may learn and recognize object texture and form boundaries. The model brings together five interacting processes: region-based texture classification, contour-based boundary grouping, surface filling-in, spatial attention, and object attention. The model shows how form boundaries can determine regions in which surface filling-in occurs; how surface filling-in interacts with spatial attention to generate a form-fitting distribution of spatial attention, or attentional shroud; how the strongest shroud can inhibit weaker shrouds; and how the winning shroud regulates learning of texture categories, and thus the allocation of object attention. The model can discriminate abutted textures with blurred boundaries and is sensitive to texture boundary attributes like discontinuities in orientation and texture flow curvature as well as to relative orientations of texture elements. The model quantitatively fits a large set of human psychophysical data on orientation-based textures. Object boundar output of the model is compared to computer vision algorithms using a set of human segmented photographic images. The model classifies textures and suppresses noise using a multiple scale oriented filterbank and a distributed Adaptive Resonance Theory (dART) classifier. The matched signal between the bottom-up texture inputs and top-down learned texture categories is utilized by oriented competitive and cooperative grouping processes to generate texture boundaries that control surface filling-in and spatial attention. Topdown modulatory attentional feedback from boundary and surface representations to early filtering stages results in enhanced texture boundaries and more efficient learning of texture within attended surface regions. Surface-based attention also provides a self-supervising training signal for learning new textures. Importance of the surface-based attentional feedback in texture learning and classification is tested using a set of textured images from the Brodatz micro-texture album. Benchmark studies vary from 95.1% to 98.6% with attention, and from 90.6% to 93.2% without attention.

3-D Vision and Figure-Ground Separation by Visual Cortex

A neural network theory of :3-D vision, called FACADE Theory, is described. The theory proposes a solution of the classical figure-ground problem for biological vision. It does so by suggesting how boundary representations and surface representations are formed within a Boundary Contour System (BCS) and a Feature Contour System (FCS). The BCS and FCS interact reciprocally to form 3-D boundary and surface representations that arc mutually consistent. Their interactions generate 3-D percepts wherein occluding and occluded object completed, and grouped. The theory clarifies how preattentive processes of 3-D perception and figure-ground separation interact reciprocally with attentive processes of spatial localization, object recognition, and visual search. A new theory of stereopsis is proposed that predicts how cells sensitive to multiple spatial frequencies, disparities, and orientations are combined by context-sensitive filtering, competition, and cooperation to form coherent BCS boundary segmentations. Several factors contribute to figure-ground pop-out, including: boundary contrast between spatially contiguous boundaries, whether due to scenic differences in luminance, color, spatial frequency, or disparity; partially ordered interactions from larger spatial scales and disparities to smaller scales and disparities; and surface filling-in restricted to regions surrounded by a connected boundary. Phenomena such as 3-D pop-out from a 2-D picture, DaVinci stereopsis, a 3-D neon color spreading, completion of partially occluded objects, and figure-ground reversals are analysed. The BCS and FCS sub-systems model aspects of how the two parvocellular cortical processing streams that join the Lateral Geniculate Nucleus to prestriate cortical area V4 interact to generate a multiplexed representation of Form-And-Color-And-Depth, or FACADE, within area V4. Area V4 is suggested to support figure-ground separation and to interact. with cortical mechanisms of spatial attention, attentive objcect learning, and visual search. Adaptive Resonance Theory (ART) mechanisms model aspects of how prestriate visual cortex interacts reciprocally with a visual object recognition system in inferotemporal cortex (IT) for purposes of attentive object learning and categorization. Object attention mechanisms of the What cortical processing stream through IT cortex are distinguished from spatial attention mechanisms of the Where cortical processing stream through parietal cortex. Parvocellular BCS and FCS signals interact with the model What stream. Parvocellular FCS and magnocellular Motion BCS signals interact with the model Where stream. Reciprocal interactions between these visual, What, and Where mechanisms arc used to discuss data about visual search and saccadic eye movements, including fast search of conjunctive targets, search of 3-D surfaces, selective search of like-colored targets, attentive tracking of multi-element groupings, and recursive search of simultaneously presented targets.

Fast Synchronization of Perpetual Grouping in Laminar Visual Cortical Circuits

Perceptual grouping is well-known to be a fundamental process during visual perception, notably grouping across scenic regions that do not receive contrastive visual inputs. Illusory contours are a classical example of such groupings. Recent psychophysical and neurophysiological evidence have shown that the grouping process can facilitate rapid synchronization of the cells that are bound together by a grouping, even when the grouping must be completed across regions that receive no contrastive inputs. Synchronous grouping can hereby bind together different object parts that may have become desynchronized due to a variety of factors, and can enhance the efficiency of cortical transmission. Neural models of perceptual grouping have clarified how such fast synchronization may occur by using bipole grouping cells, whose predicted properties have been supported by psychophysical, anatomical, and neurophysiological experiments. These models have not, however, incorporated some of the realistic constraints on which groupings in the brain are conditioned, notably the measured spatial extent of long-range interactions in layer 2/3 of a grouping network, and realistic synaptic and axonal signaling delays within and across cells in different cortical layers. This work addresses the question: Can long-range interactions that obey the bipole constraint achieve fast synchronization under realistic anatomical and neurophysiological constraints that initially desynchronize grouping signals? Can the cells that synchronize retain their analog sensitivity to changing input amplitudes? Can the grouping process complete and synchronize illusory contours across gaps in bottom-up inputs? Our simulations show that the answer to these questions is Yes.

Laminar Cortical Dynamics of Cognitive and Motor Working Memory, Sequence Learning and Performance: Toward a Unified Theory of How the Cerebral Cortex Works

How do the layered circuits of prefrontal and motor cortex carry out working memory storage, sequence learning, and voluntary sequential item selection and performance? A neural model called LIST PARSE is presented to explain and quantitatively simulate cognitive data about both immediate serial recall and free recall, including bowing of the serial position performance curves, error-type distributions, temporal limitations upon recall, and list length effects. The model also qualitatively explains cognitive effects related to attentional modulation, temporal grouping, variable presentation rates, phonemic similarity, presentation of non-words, word frequency/item familiarity and list strength, distracters and modality effects. In addition, the model quantitatively simulates neurophysiological data from the macaque prefrontal cortex obtained during sequential sensory-motor imitation and planned performance. The article further develops a theory concerning how the cerebral cortex works by showing how variations of the laminar circuits that have previously clarified how the visual cortex sees can also support cognitive processing of sequentially organized behaviors.

Multi-Area Visuotopic Map Complexes in Macaque Striate and Extra-striate Cortex

We propose that a simple, closed-form mathematical expression--the Wedge-Dipole mapping--provides a concise approximation to the full-field, two-dimensional topographic structure of macaque V1, V2, and V3. A single map function, which we term a map complex, acts as a simultaneous descriptor of all three areas. Quantitative estimation of the Wedge-Dipole parameters is provided via 2DG data of central-field V1 topography and a publicly available data set of full-field macaque V1 and V2 topography. Good quantitative agreement is obtained between the data and the model presented here. The increasing importance of fMRI-based brain imaging motivates the development of more sophisticated two-dimensional models of cortical visuotopy, in contrast to the one-dimensional approximations that have been in common use. One reason is that topography has traditionally supplied an important aspect of "ground truth", or validation, for brain imaging, suggesting that further development of high-resolution fMRI will be facilitated by this data analysis. In addition, several important insights into the nature of cortical topography follows from this work. The presence of anisotropy in cortical magnification factor is shown to follow mathematically from the shared boundary conditions at the V1-V2 and V2-V3 borders, and therefore may not causally follow from the existence of columnar systems in these areas, as is widely assumed. An application of the Wedge-Dipole model to localizing aspects of visual processing to specific cortical areas--extending previous work in correlating V1 cortical magnification factor to retinal anatomy or visual psychophysics data--is briefly discussed.

Cortical Dynamics of Visual Motion Perception: Short-Range and Long Range Apparent Motion

This article describes further evidence for a new neural network theory of biological motion perception that is called a Motion Boundary Contour System. This theory clarifies why parallel streams Vl-> V2 and Vl-> MT exist for static form and motion form processing among the areas Vl, V2, and MT of visual cortex. The Motion Boundary Contour System consists of several parallel copies, such that each copy is activated by a different range of receptive field sizes. Each copy is further subdivided into two hierarchically organized subsystems: a Motion Oriented Contrast Filter, or MOC Filter, for preprocessing moving images; and a Cooperative-Competitive Feedback Loop, or CC Loop, for generating emergent boundary segmentations of the filtered signals. The present article uses the MOC Filter to explain a variety of classical and recent data about short-range and long-range apparent motion percepts that have not yet been explained by alternative models. These data include split motion; reverse-contrast gamma motion; delta motion; visual inertia; group motion in response to a reverse-contrast Ternus display at short interstimulus intervals; speed-up of motion velocity as interfiash distance increases or flash duration decreases; dependence of the transition from element motion to group motion on stimulus duration and size; various classical dependencies between flash duration, spatial separation, interstimulus interval, and motion threshold known as Korte's Laws; and dependence of motion strength on stimulus orientation and spatial frequency. These results supplement earlier explanations by the model of apparent motion data that other models have not explained; a recent proposed solution of the global aperture problem, including explanations of motion capture and induced motion; an explanation of how parallel cortical systems for static form perception and motion form perception may develop, including a demonstration that these parallel systems are variations on a common cortical design; an explanation of why the geometries of static form and motion form differ, in particular why opposite orientations differ by 90°, whereas opposite directions differ by 180°, and why a cortical stream Vl -> V2 -> MT is needed; and a summary of how the main properties of other motion perception models can be assimilated into different parts of the Motion Boundary Contour System design.

Synchronized Oscillations During Cooperative Feature Lining in a Cortical Model of Visual Perception

A neural network model of synchronized oscillations in visual cortex is presented to account for recent neurophysiological findings that such synchronization may reflect global properties of the stimulus. In these experiments, synchronization of oscillatory firing responses to moving bar stimuli occurred not only for nearby neurons, but also occurred between neurons separated by several cortical columns (several mm of cortex) when these neurons shared some receptive field preferences specific to the stimuli. These results were obtained for single bar stimuli and also across two disconnected, but colinear, bars moving in the same direction. Our model and computer simulations obtain these synchrony results across both single and double bar stimuli using different, but formally related, models of preattentive visual boundary segmentation and attentive visual object recognition, as well as nearest-neighbor and randomly coupled models.

Cortical Dynamics of Visual Motion Perception: Short-Range and Long-Range Apparent Motion

This article describes further evidence for a new neural network theory of biological motion perception. The theory clarifies why parallel streams Vl --> V2, Vl --> MT, and Vl --> V2 --> MT exist for static form and motion form processing among the areas Vl, V2, and MT of visual cortex. The theory suggests that the static form system (Static BCS) generates emergent boundary segmentations whose outputs are insensitive to direction-ofcontrast and insensitive to direction-of-motion, whereas the motion form system (Motion BCS) generates emergent boundary segmentations whose outputs are insensitive to directionof-contrast but sensitive to direction-of-motion. The theory is used to explain classical and recent data about short-range and long-range apparent motion percepts that have not yet been explained by alternative models. These data include beta motion; split motion; gamma motion and reverse-contrast gamma motion; delta motion; visual inertia; the transition from group motion to element motion in response to a Ternus display as the interstimulus interval (ISI) decreases; group motion in response to a reverse-contrast Ternus display even at short ISIs; speed-up of motion velocity as interflash distance increases or flash duration decreases; dependence of the transition from element motion to group motion on stimulus duration and size; various classical dependencies between flash duration, spatial separation, ISI, and motion threshold known as Korte's Laws; dependence of motion strength on stimulus orientation and spatial frequency; short-range and long-range form-color interactions; and binocular interactions of flashes to different eyes.

Synchronized Oscillations During Cooperative Feature Linking in a Cortical Model of Visual Perception

A neural network model of synchronized oscillator activity in visual cortex is presented in order to account for recent neurophysiological findings that such synchronization may reflect global properties of the stimulus. In these recent experiments, it was reported that synchronization of oscillatory firing responses to moving bar stimuli occurred not only for nearby neurons, but also occurred between neurons separated by several cortical columns (several mm of cortex) when these neurons shared some receptive field preferences specific to the stimuli. These results were obtained not only for single bar stimuli but also across two disconnected, but colinear, bars moving in the same direction. Our model and computer simulations obtain these synchrony results across both single and double bar stimuli. For the double bar case, synchronous oscillations are induced in the region between the bars, but no oscillations are induced in the regions beyond the stimuli. These results were achieved with cellular units that exhibit limit cycle oscillations for a robust range of input values, but which approach an equilibrium state when undriven. Single and double bar synchronization of these oscillators was achieved by different, but formally related, models of preattentive visual boundary segmentation and attentive visual object recognition, as well as nearest-neighbor and randomly coupled models. In preattentive visual segmentation, synchronous oscillations may reflect the binding of local feature detectors into a globally coherent grouping. In object recognition, synchronous oscillations may occur during an attentive resonant state that triggers new learning. These modelling results support earlier theoretical predictions of synchronous visual cortical oscillations and demonstrate the robustness of the mechanisms capable of generating synchrony.

Cortical Dynamics of Feature Binding and Reset: Control of Visual Persistence

An analysis of the reset of visual cortical circuits responsible for the binding or segmentation of visual features into coherent visual forms yields a model that explains properties of visual persistence. The reset mechanisms prevent massive smearing or visual percepts in response to rapidly moving images. The model simulates relationships among psychophysical data showing inverse relations of persistence to flash luminance and duration, greaterr persistence of illusory contours than real contours, a U-shaped temporal function for persistence of illusory contours, a reduction of persistence: due to adaptation with a stimulus of like orientation, an increase or persistence due to adaptation with a stimulus of perpendicular orientation, and an increase of persistence with spatial separation of a masking stimulus. The model suggests that a combination of habituative, opponent, and endstopping mechanisms prevent smearing and limit persistence. Earlier work with the model has analyzed data about boundary formation, texture segregation, shape-from-shading, and figure-ground separation. Thus, several types of data support each model mechanism and new predictions are made.

Laminar Cortical Dynamics of 3D Surface Perception: Stratification, transparency, and Neon Color Spreading

How does the laminar organization of cortical circuitry in areas VI and V2 give rise to 3D percepts of stratification, transparency, and neon color spreading in response to 2D pictures and 3D scenes? Psychophysical experiments have shown that such 3D percepts are sensitive to whether contiguous image regions have the same relative contrast polarity (dark-light or lightdark), yet long-range perceptual grouping is known to pool over opposite contrast polarities. The ocularity of contiguous regions is also critical for neon color spreading: Having different ocularity despite the contrast relationship that favors neon spreading blocks the spread. In addition, half visible points in a stereogram can induce near-depth transparency if the contrast relationship favors transparency in the half visible areas. It thus seems critical to have the whole contrast relationship in a monocular configuration, since splitting it between two stereogram images cancels the effect. What adaptive functions of perceptual grouping enable it to both preserve sensitivity to monocular contrast and also to pool over opposite contrasts? Aspects of cortical development, grouping, attention, perceptual learning, stereopsis and 3D planar surface perception have previously been analyzed using a 3D LAMINART model of cortical areas VI, V2, and V4. The present work consistently extends this model to show how like-polarity competition between VI simple cells in layer 4 may be combined with other LAMINART grouping mechanisms, such as cooperative pooling of opposite polarities at layer 2/3 complex cells. The model also explains how the Metelli Rules can lead to transparent percepts, how bistable transparency percepts can arise in which either surface can be perceived as transparent, and how such a transparency reversal can be facilitated by an attention shift. The like-polarity inhibition prediction is consistent with lateral masking experiments in which two f1anking Gabor patches with the same contrast polarity as the target increase the target detection threshold when they approach the target. It is also consistent with LAMINART simulations of cortical development. Other model explanations and testable predictions will also be presented.