Linking Visual Development and Learning to Information Processing: Preattentive and Attentive Brain Dynamics

National Science Foundation (SBE-0354378); Office of Naval Research (N00014-95-1-0657)

Space, Time and Learning in the Hippocampus: How Fine Spatial and Temporal Scales Are Expanded into Population Codes for Behavioral Control

The hippocampus participates in multiple functions, including spatial navigation, adaptive timing, and declarative (notably, episodic) memory. How does it carry out these particular functions? The present article proposes that hippocampal spatial and temporal processing are carried out by parallel circuits within entorhinal cortex, dentate gyrus, and CA3 that are variations of the same circuit design. In particular, interactions between these brain regions transform fine spatial and temporal scales into population codes that are capable of representing the much larger spatial and temporal scales that are needed to control adaptive behaviors. Previous models of adaptively timed learning propose how a spectrum of cells tuned to brief but different delays are combined and modulated by learning to create a population code for controlling goal-oriented behaviors that span hundreds of milliseconds or even seconds. Here it is proposed how projections from entorhinal grid cells can undergo a similar learning process to create hippocampal place cells that can cover a space of many meters that are needed to control navigational behaviors. The suggested homology between spatial and temporal processing may clarify how spatial and temporal information may be integrated into an episodic memory.

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.

Towards a Unified Theory of Neocortex: Laminar Cortical Circuits for Vision and Cognition

A key goal of computational neuroscience is to link brain mechanisms to behavioral functions. The present article describes recent progress towards explaining how laminar neocortical circuits give rise to biological intelligence. These circuits embody two new and revolutionary computational paradigms: Complementary Computing and Laminar Computing. Circuit properties include a novel synthesis of feedforward and feedback processing, of digital and analog processing, and of pre-attentive and attentive processing. This synthesis clarifies the appeal of Bayesian approaches but has a far greater predictive range that naturally extends to self-organizing processes. Examples from vision and cognition are summarized. A LAMINART architecture unifies properties of visual development, learning, perceptual grouping, attention, and 3D vision. A key modeling theme is that the mechanisms which enable development and learning to occur in a stable way imply properties of adult behavior. It is noted how higher-order attentional constraints can influence multiple cortical regions, and how spatial and object attention work together to learn view-invariant object categories. In particular, a form-fitting spatial attentional shroud can allow an emerging view-invariant object category to remain active while multiple view categories are associated with it during sequences of saccadic eye movements. Finally, the chapter summarizes recent work on the LIST PARSE model of cognitive information processing by the laminar circuits of prefrontal cortex. LIST PARSE models the short-term storage of event sequences in working memory, their unitization through learning into sequence, or list, chunks, and their read-out in planned sequential performance that is under volitional control. LIST PARSE provides a laminar embodiment of Item and Order working memories, also called Competitive Queuing models, that have been supported by both psychophysical and neurobiological data. These examples show how variations of a common laminar cortical design can embody properties of visual and cognitive intelligence that seem, at least on the surface, to be mechanistically unrelated.

Simultaneous Learning of Nonlinear Manifold and Dynamical Models for High-dimensional Time Series

The goal of this work is to learn a parsimonious and informative representation for high-dimensional time series. Conceptually, this comprises two distinct yet tightly coupled tasks: learning a low-dimensional manifold and modeling the dynamical process. These two tasks have a complementary relationship as the temporal constraints provide valuable neighborhood information for dimensionality reduction and conversely, the low-dimensional space allows dynamics to be learnt efficiently. Solving these two tasks simultaneously allows important information to be exchanged mutually. If nonlinear models are required to capture the rich complexity of time series, then the learning problem becomes harder as the nonlinearities in both tasks are coupled. The proposed solution approximates the nonlinear manifold and dynamics using piecewise linear models. The interactions among the linear models are captured in a graphical model. By exploiting the model structure, efficient inference and learning algorithms are obtained without oversimplifying the model of the underlying dynamical process. Evaluation of the proposed framework with competing approaches is conducted in three sets of experiments: dimensionality reduction and reconstruction using synthetic time series, video synthesis using a dynamic texture database, and human motion synthesis, classification and tracking on a benchmark data set. In all experiments, the proposed approach provides superior performance.

Simultaneous Learning of Non-Linear Manifold and Dynamical Models for High-Dimensional Time Series

The goal of this work is to learn a parsimonious and informative representation for high-dimensional time series. Conceptually, this comprises two distinct yet tightly coupled tasks: learning a low-dimensional manifold and modeling the dynamical process. These two tasks have a complementary relationship as the temporal constraints provide valuable neighborhood information for dimensionality reduction and conversely, the low-dimensional space allows dynamics to be learnt efficiently. Solving these two tasks simultaneously allows important information to be exchanged mutually. If nonlinear models are required to capture the rich complexity of time series, then the learning problem becomes harder as the nonlinearities in both tasks are coupled. The proposed solution approximates the nonlinear manifold and dynamics using piecewise linear models. The interactions among the linear models are captured in a graphical model. The model structure setup and parameter learning are done using a variational Bayesian approach, which enables automatic Bayesian model structure selection, hence solving the problem of over-fitting. By exploiting the model structure, efficient inference and learning algorithms are obtained without oversimplifying the model of the underlying dynamical process. Evaluation of the proposed framework with competing approaches is conducted in three sets of experiments: dimensionality reduction and reconstruction using synthetic time series, video synthesis using a dynamic texture database, and human motion synthesis, classification and tracking on a benchmark data set. In all experiments, the proposed approach provides superior performance.

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.

Spikes, Synchrony, and Attentive Learning by Laminar Thalamocortical Circuits

This article develops the Synchronous Matching Adaptive Resonance Theory (SMART) neural model to explain how the brain may coordinate multiple levels of thalamocortical and corticocortical processing to rapidly learn, and stably remember, important information about a changing world. The model clarifies how bottom-up and top-down processes work together to realize this goal, notably how processes of learning, expectation, attention, resonance, and synchrony are coordinated. The model hereby clarifies, for the first time, how the following levels of brain organization coexist to realize cognitive processing properties that regulate fast learning and stable memory of brain representations: single cell properties, such as spiking dynamics, spike-timing-dependent plasticity (STDP), and acetylcholine modulation; detailed laminar thalamic and cortical circuit designs and their interactions; aggregate cell recordings, such as current-source densities and local field potentials; and single cell and large-scale inter-areal oscillations in the gamma and beta frequency domains. In particular, the model predicts how laminar circuits of multiple cortical areas interact with primary and higher-order specific thalamic nuclei and nonspecific thalamic nuclei to carry out attentive visual learning and information processing. The model simulates how synchronization of neuronal spiking occurs within and across brain regions, and triggers STDP. Matches between bottom-up adaptively filtered input patterns and learned top-down expectations cause gamma oscillations that support attention, resonance, and learning. Mismatches inhibit learning while causing beta oscillations during reset and hypothesis testing operations that are initiated in the deeper cortical layers. The generality of learned recognition codes is controlled by a vigilance process mediated by acetylcholine.

Simulating Effects of Learning and Lesions with a Model of Intrinsic and Synaptically Gated Responses of Striatal Cholinergic Interneurons

The giant cholinergic interneurons of the striatum are tonically active neurons (TANs) that respond with characteristic pauses to novel events and to appetitive and aversive conditioned stimuli. Fluctuations in acetylcholine release by TANs modulate performance- and learning-related dynamics in the striatum. Whereas tonic activity emerges from intrinsic properties of these neurons, glutamatergic inputs from thalamic centromedian-parafascicular nuclei, and dopaminergic inputs from midbrain, are required for the generation of pause responses. No prior computational models encompass both intrinsic and synaptically-gated dynamics. We present a mathematical model that robustly accounts for behavior-related electrophysiological properties of TANs in terms of their intrinsic physiological properties and known afferents. In the model, balanced intrinsic hyperpolarizing and depolarizing currents engender tonic firing, and glutamatergic inputs from thalamus (and cortex) both directly excite and indirectly inhibit TANs. If the latter inhibition, presumably mediated by GABAergic interneurons, exceeds a threshold, its effect is amplified by a KIR current to generate a prolonged pause. In the model, the intrinsic mechanisms and external inputs are both modulated by learning-dependent dopamine (DA) signals and our simulations revealed that many learning-dependent behaviors of TANs are explicable without recourse to learning-dependent changes in synapses onto TANs. The "teaching signal" that modulates reinforcement learning at cortico-striatal synapses may be a sequence composed of an adaptively scaled DA burst, a brief ACh burst, and a scaled ACh pause. Such an interpretation is consistent with recent data on cholinergic control of LTD of cortical synapses onto striatal spiny projection neurons.

Vector Associative Maps: Unsupervised Real-time Error-based Learning and Control of Movement Trajectories

This article describes neural network models for adaptive control of arm movement trajectories during visually guided reaching and, more generally, a framework for unsupervised real-time error-based learning. The models clarify how a child, or untrained robot, can learn to reach for objects that it sees. Piaget has provided basic insights with his concept of a circular reaction: As an infant makes internally generated movements of its hand, the eyes automatically follow this motion. A transformation is learned between the visual representation of hand position and the motor representation of hand position. Learning of this transformation eventually enables the child to accurately reach for visually detected targets. Grossberg and Kuperstein have shown how the eye movement system can use visual error signals to correct movement parameters via cerebellar learning. Here it is shown how endogenously generated arm movements lead to adaptive tuning of arm control parameters. These movements also activate the target position representations that are used to learn the visuo-motor transformation that controls visually guided reaching. The AVITE model presented here is an adaptive neural circuit based on the Vector Integration to Endpoint (VITE) model for arm and speech trajectory generation of Bullock and Grossberg. In the VITE model, a Target Position Command (TPC) represents the location of the desired target. The Present Position Command (PPC) encodes the present hand-arm configuration. The Difference Vector (DV) population continuously.computes the difference between the PPC and the TPC. A speed-controlling GO signal multiplies DV output. The PPC integrates the (DV)·(GO) product and generates an outflow command to the arm. Integration at the PPC continues at a rate dependent on GO signal size until the DV reaches zero, at which time the PPC equals the TPC. The AVITE model explains how self-consistent TPC and PPC coordinates are autonomously generated and learned. Learning of AVITE parameters is regulated by activation of a self-regulating Endogenous Random Generator (ERG) of training vectors. Each vector is integrated at the PPC, giving rise to a movement command. The generation of each vector induces a complementary postural phase during which ERG output stops and learning occurs. Then a new vector is generated and the cycle is repeated. This cyclic, biphasic behavior is controlled by a specialized gated dipole circuit. ERG output autonomously stops in such a way that, across trials, a broad sample of workspace target positions is generated. When the ERG shuts off, a modulator gate opens, copying the PPC into the TPC. Learning of a transformation from TPC to PPC occurs using the DV as an error signal that is zeroed due to learning. This learning scheme is called a Vector Associative Map, or VAM. The VAM model is a general-purpose device for autonomous real-time error-based learning and performance of associative maps. The DV stage serves the dual function of reading out new TPCs during performance and reading in new adaptive weights during learning, without a disruption of real-time operation. YAMs thus provide an on-line unsupervised alternative to the off-line properties of supervised error-correction learning algorithms. YAMs and VAM cascades for learning motor-to-motor and spatial-to-motor maps are described. YAM models and Adaptive Resonance Theory (ART) models exhibit complementary matching, learning, and performance properties that together provide a foundation for designing a total sensory-cognitive and cognitive-motor autonomous system.