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.

AIRSTREAM: A Neural Network Model of Auditory Scene Analysis and Source Segregation

Multiple sound sources often contain harmonics that overlap and may be degraded by environmental noise. The auditory system is capable of teasing apart these sources into distinct mental objects, or streams. Such an "auditory scene analysis" enables the brain to solve the cocktail party problem. A neural network model of auditory scene analysis, called the AIRSTREAM model, is presented to propose how the brain accomplishes this feat. The model clarifies how the frequency components that correspond to a give acoustic source may be coherently grouped together into distinct streams based on pitch and spatial cues. The model also clarifies how multiple streams may be distinguishes and seperated by the brain. Streams are formed as spectral-pitch resonances that emerge through feedback interactions between frequency-specific spectral representaion of a sound source and its pitch. First, the model transforms a sound into a spatial pattern of frequency-specific activation across a spectral stream layer. The sound has multiple parallel representations at this layer. A sound's spectral representation activates a bottom-up filter that is sensitive to harmonics of the sound's pitch. The filter activates a pitch category which, in turn, activate a top-down expectation that allows one voice or instrument to be tracked through a noisy multiple source environment. Spectral components are suppressed if they do not match harmonics of the top-down expectation that is read-out by the selected pitch, thereby allowing another stream to capture these components, as in the "old-plus-new-heuristic" of Bregman. Multiple simultaneously occuring spectral-pitch resonances can hereby emerge. These resonance and matching mechanisms are specialized versions of Adaptive Resonance Theory, or ART, which clarifies how pitch representations can self-organize durin learning of harmonic bottom-up filters and top-down expectations. The model also clarifies how spatial location cues can help to disambiguate two sources with similar spectral cures. Data are simulated from psychophysical grouping experiments, such as how a tone sweeping upwards in frequency creates a bounce percept by grouping with a downward sweeping tone due to proximity in frequency, even if noise replaces the tones at their interection point. Illusory auditory percepts are also simulated, such as the auditory continuity illusion of a tone continuing through a noise burst even if the tone is not present during the noise, and the scale illusion of Deutsch whereby downward and upward scales presented alternately to the two ears are regrouped based on frequency proximity, leading to a bounce percept. Since related sorts of resonances have been used to quantitatively simulate psychophysical data about speech perception, the model strengthens the hypothesis the ART-like mechanisms are used at multiple levels of the auditory system. Proposals for developing the model to explain more complex streaming data are also provided.

Neural Modeling and Imaging of the Cortical Interactions Underlying Syllable Production

This paper describes a neural model of speech acquisition and production that accounts for a wide range of acoustic, kinematic, and neuroimaging data concerning the control of speech movements. The model is a neural network whose components correspond to regions of the cerebral cortex and cerebellum, including premotor, motor, auditory, and somatosensory cortical areas. Computer simulations of the model verify its ability to account for compensation to lip and jaw perturbations during speech. Specific anatomical locations of the model's components are estimated, and these estimates are used to simulate fMRI experiments of simple syllable production with and without jaw perturbations.

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.

Target Selection by Frontal Cortex During Coordinated Saccadic and Smooth Pursuit Eye Movement

Oculomotor tracking of moving objects is an important component of visually based cognition and planning. Such tracking is achieved by a combination of saccades and smooth pursuit eye movements. In particular, the saccadic and smooth pursuit systems interact to often choose the same target, and to maximize its visibility through time. How do multiple brain regions interact, including frontal cortical areas, to decide the choice of a target among several competing moving stimuli? How is target selection information that is created by a bias (e.g., electrical stimulation) transferred from one movement system to another? These saccade-pursuit interactions are clarified by a new computational neural model, which describes interactions among motion processing areas MT, MST, FPA, DLPN; saccade specification, selection, and planning areas LIP, FEF, SNr, SC; the saccadic generator in the brain stem; and the cerebellum. Model simulations explain a broad range of neuroanatomical and neurophysiological data. These results are in contrast with the simplest parallel model with no interactions between saccades and pursuit than common-target selection and recruitment of shared motoneurons. Actual tracking episodes in primates reveal multiple systematic deviations from predictions of the simplest parallel model, which are explained by the current model.

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.

Brain Learning and Recognition: The Large and the Small of It in Inferotemporal Cortex

Anterior inferotemporal cortex (ITa) plays a key role in visual object recognition. Recognition is tolerant to object position, size, and view changes, yet recent neurophysiological data show ITa cells with high object selectivity often have low position tolerance, and vice versa. A neural model learns to simulate both this tradeoff and ITa responses to image morphs using large-scale and small-scale IT cells whose population properties may support invariant recognition.

Grid Cell Hexagonal Patterns Formed by Fast Self-Organized Learning within Entorhinal Cortex

Grid cells in the dorsal segment of the medial entorhinal cortex (dMEC) show remarkable hexagonal activity patterns, at multiple spatial scales, during spatial navigation. How these hexagonal patterns arise has excited intense interest. It has previously been shown how a selforganizing map can convert firing patterns across entorhinal grid cells into hippocampal place cells that are capable of representing much larger spatial scales. Can grid cell firing fields also arise during navigation through learning within a self-organizing map? A neural model is proposed that converts path integration signals into hexagonal grid cell patterns of multiple scales. This GRID model creates only grid cell patterns with the observed hexagonal structure, predicts how these hexagonal patterns can be learned from experience, and can process biologically plausible neural input and output signals during navigation. These results support a unified computational framework for explaining how entorhinal-hippocampal interactions support spatial navigation.

Parallel Auditory Filtering By Sustained and Transient Channels Separates Coarticulated Vowels and Consonants

A neural model of peripheral auditory processing is described and used to separate features of coarticulated vowels and consonants. After preprocessing of speech via a filterbank, the model splits into two parallel channels, a sustained channel and a transient channel. The sustained channel is sensitive to relatively stable parts of the speech waveform, notably synchronous properties of the vocalic portion of the stimulus it extends the dynamic range of eighth nerve filters using coincidence deteectors that combine operations of raising to a power, rectification, delay, multiplication, time averaging, and preemphasis. The transient channel is sensitive to critical features at the onsets and offsets of speech segments. It is built up from fast excitatory neurons that are modulated by slow inhibitory interneurons. These units are combined over high frequency and low frequency ranges using operations of rectification, normalization, multiplicative gating, and opponent processing. Detectors sensitive to frication and to onset or offset of stop consonants and vowels are described. Model properties are characterized by mathematical analysis and computer simulations. Neural analogs of model cells in the cochlear nucleus and inferior colliculus are noted, as are psychophysical data about perception of CV syllables that may be explained by the sustained transient channel hypothesis. The proposed sustained and transient processing seems to be an auditory analog of the sustained and transient processing that is known to occur in vision.

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.

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.