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.

A Quantitative Evaluation of the AVITEWRITE Model of Handwriting Learning

Much sensory-motor behavior develops through imitation, as during the learning of handwriting by children. Such complex sequential acts are broken down into distinct motor control synergies, or muscle groups, whose activities overlap in time to generate continuous, curved movements that obey an intense relation between curvature and speed. The Adaptive Vector Integration to Endpoint (AVITEWRITE) model of Grossberg and Paine (2000) proposed how such complex movements may be learned through attentive imitation. The model suggest how frontal, parietal, and motor cortical mechanisms, such as difference vector encoding, under volitional control from the basal ganglia, interact with adaptively-timed, predictive cerebellar learning during movement imitation and predictive performance. Key psycophysical and neural data about learning to make curved movements were simulated, including a decrease in writing time as learning progresses; generation of unimodal, bell-shaped velocity profiles for each movement synergy; size scaling with isochrony, and speed scaling with preservation of the letter shape and the shapes of the velocity profiles; an inverse relation between curvature and tangential velocity; and a Two-Thirds Power Law relation between angular velocity and curvature. However, the model learned from letter trajectories of only one subject, and only qualitative kinematic comparisons were made with previously published human data. The present work describes a quantitative test of AVITEWRITE through direct comparison of a corpus of human handwriting data with the model's performance when it learns by tracing human trajectories. The results show that model performance was variable across subjects, with an average correlation between the model and human data of 89+/-10%. The present data from simulations using the AVITEWRITE model highlight some of its strengths while focusing attention on areas, such as novel shape learning in children, where all models of handwriting and learning of other complex sensory-motor skills would benefit from further research.

Learning and Production of Movement Sequences: Behavioral, Neurophysiological, and Modeling Perspectives

A growing wave of behavioral studies, using a wide variety of paradigms that were introduced or greatly refined in recent years, has generated a new wealth of parametric observations about serial order behavior. What was a mere trickle of neurophysiological studies has grown to a more steady stream of probes of neural sites and mechanisms underlying sequential behavior. Moreover, simulation models of serial behavior generation have begun to open a channel to link cellular dynamics with cognitive and behavioral dynamics. Here we summarize the major results from prominent sequence learning and performance tasks, namely immediate serial recall, typing, 2XN, discrete sequence production, and serial reaction time. These populate a continuum from higher to lower degrees of internal control of sequential organization. The main movement classes covered are speech and keypressing, both involving small amplitude movements that are very amenable to parametric study. A brief synopsis of classes of serial order models, vis-à-vis the detailing of major effects found in the behavioral data, leads to a focus on competitive queuing (CQ) models. Recently, the many behavioral predictive successes of CQ models have been joined by successful prediction of distinctively patterend electrophysiological recordings in prefrontal cortex, wherein parallel activation dynamics of multiple neural ensembles strikingly matches the parallel dynamics predicted by CQ theory. An extended CQ simulation model-the N-STREAMS neural network model-is then examined to highlight issues in ongoing attemptes to accomodate a broader range of behavioral and neurophysiological data within a CQ-consistent theory. Important contemporary issues such as the nature of working memory representations for sequential behavior, and the development and role of chunks in hierarchial control are prominent throughout.

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)

KInNeSS: A Modular Framework for Computational Neuroscience

Making use of very detailed neurophysiological, anatomical, and behavioral data to build biological-realistic computational models of animal behavior is often a difficult task. Until recently, many software packages have tried to resolve this mismatched granularity with different approaches. This paper presents KInNeSS, the KDE Integrated NeuroSimulation Software environment, as an alternative solution to bridge the gap between data and model behavior. This open source neural simulation software package provides an expandable framework incorporating features such as ease of use, scalabiltiy, an XML based schema, and multiple levels of granularity within a modern object oriented programming design. KInNeSS is best suited to simulate networks of hundreds to thousands of branched multu-compartmental neurons with biophysical properties such as membrane potential, voltage-gated and ligand-gated channels, the presence of gap junctions of ionic diffusion, neuromodulation channel gating, the mechanism for habituative or depressive synapses, axonal delays, and synaptic plasticity. KInNeSS outputs include compartment membrane voltage, spikes, local-field potentials, and current source densities, as well as visualization of the behavior of a simulated agent. An explanation of the modeling philosophy and plug-in development is also presented. Further developement of KInNeSS is ongoing with the ultimate goal of creating a modular framework that will help researchers across different disciplines to effecitively collaborate using a modern neural simulation platform.

Adaptation of Dopamine Neurons' Mismatch Sensitivity Is not Compatible With Reinforcement Learning Theory

Recent electrophysical data inspired the claim that dopaminergic neurons adapt their mismatch sensitivities to reflect variances of expected rewards. This contradicts reward prediction error theory and most basal ganglia models. Application of learning principles points to a testable alternative interpretation-of the same data-that is compatible with existing theory.

View-Invariant Object Category Learning, Recognition, and Search: How Spatial and Object Attention Are Coordinated Using Surface-Based Attentional Shrouds

Air Force Office of Scientific Research (F49620-01-1-0397); National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624)

SOVEREIGN: An Autonomous Neural System for Incrementally Learning Planned Action Sequence to Navigate Towards a Rewarded Goal

How do reactive and planned behaviors interact in real time? How are sequences of such behaviors released at appropriate times during autonomous navigation to realize valued goals? Controllers for both animals and mobile robots, or animats, need reactive mechanisms for exploration, and learned plans to reach goal objects once an environment becomes familiar. The SOVEREIGN (Self-Organizing, Vision, Expectation, Recognition, Emotion, Intelligent, Goaloriented Navigation) animat model embodies these capabilities, and is tested in a 3D virtual reality environment. SOVEREIGN includes several interacting subsystems which model complementary properties of cortical What and Where processing streams and which clarify similarities between mechanisms for navigation and arm movement control. As the animat explores an environment, visual inputs are processed by networks that are sensitive to visual form and motion in the What and Where streams, respectively. Position-invariant and sizeinvariant recognition categories are learned by real-time incremental learning in the What stream. Estimates of target position relative to the animat are computed in the Where stream, and can activate approach movements toward the target. Motion cues from animat locomotion can elicit head-orienting movements to bring a new target into view. Approach and orienting movements are alternately performed during animat navigation. Cumulative estimates of each movement are derived from interacting proprioceptive and visual cues. Movement sequences are stored within a motor working memory. Sequences of visual categories are stored in a sensory working memory. These working memories trigger learning of sensory and motor sequence categories, or plans, which together control planned movements. Predictively effective chunk combinations are selectively enhanced via reinforcement learning when the animat is rewarded. Selected planning chunks effect a gradual transition from variable reactive exploratory movements to efficient goal-oriented planned movement sequences. Volitional signals gate interactions between model subsystems and the release of overt behaviors. The model can control different motor sequences under different motivational states and learns more efficient sequences to rewarded goals as exploration proceeds.

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.

KInNeSS: A Modular Framework for Computational Neuroscience

Making use of very detailed neurophysiological, anatomical, and behavioral data to build biologically-realistic computational models of animal behavior is often a difficult task. Until recently, many software packages have tried to resolve this mismatched granularity with different approaches. This paper presents KInNeSS, the KDE Integrated NeuroSimulation Software environment, as an alternative solution to bridge the gap between data and model behavior. This open source neural simulation software package provides an expandable framework incorporating features such as ease of use, scalability, an XML based schema, and multiple levels of granularity within a modern object oriented programming design. KInNeSS is best suited to simulate networks of hundreds to thousands of branched multi-compartmental neurons with biophysical properties such as membrane potential, voltage-gated and ligand-gated channels, the presence of gap junctions or ionic diffusion, neuromodulation channel gating, the mechanism for habituative or depressive synapses, axonal delays, and synaptic plasticity. KInNeSS outputs include compartment membrane voltage, spikes, local-field potentials, and current source densities, as well as visualization of the behavior of a simulated agent. An explanation of the modeling philosophy and plug-in development is also presented. Further development of KInNeSS is ongoing with the ultimate goal of creating a modular framework that will help researchers across different disciplines to effectively collaborate using a modern neural simulation platform.

Cortical Learning of Recognition Categories: A Resolution of the Exemplar Vs. Prototype Debate

Do humans and animals learn exemplars or prototypes when they categorize objects and events in the world? How are different degrees of abstraction realized through learning by neurons in inferotemporal and prefrontal cortex? How do top-down expectations influence the course of learning? Thirty related human cognitive experiments (the 5-4 category structure) have been used to test competing views in the prototype-exemplar debate. In these experiments, during the test phase, subjects unlearn in a characteristic way items that they had learned to categorize perfectly in the training phase. Many cognitive models do not describe how an individual learns or forgets such categories through time. Adaptive Resonance Theory (ART) neural models provide such a description, and also clarify both psychological and neurobiological data. Matching of bottom-up signals with learned top-down expectations plays a key role in ART model learning. Here, an ART model is used to learn incrementally in response to 5-4 category structure stimuli. Simulation results agree with experimental data, achieving perfect categorization in training and a good match to the pattern of errors exhibited by human subjects in the testing phase. These results show how the model learns both prototypes and certain exemplars in the training phase. ART prototypes are, however, unlike the ones posited in the traditional prototype-exemplar debate. Rather, they are critical patterns of features to which a subject learns to pay attention based on past predictive success and the order in which exemplars are experienced. Perturbations of old memories by newly arriving test items generate a performance curve that closely matches the performance pattern of human subjects. The model also clarifies exemplar-based accounts of data concerning amnesia.

Neural Dynamics of Motion Perception, Recognition Learning, and Spatial Attention

Advanced Research Projects Agency (ONR N00014-92-J-4015); National Science Foundation (IRI-90-24877); Office of Naval Research (N00014-91-J-4100)

Learning Temporal Contexts and Priming-Preparation Modes for Pattern Recognition

The system presented here is based on neurophysiological and electrophysiological data. It computes three types of increasingly integrated temporal and probability contexts, in a bottom-up mode. To each of these contexts corresponds an increasingly specific top-down priming effect on lower processing stages, mostly pattern recognition and discrimination. Contextual learning of time intervals, events' temporal order or sequential dependencies and events' prior probability results from the delivery of large stimuli sequences. This learning gives rise to emergent properties which closely match the experimental data.

A Self-Organizing Neural Network for Learning a Body-Centered Invariant Representation of 3-D Target Position

This paper describes a self-organizing neural network that rapidly learns a body-centered representation of 3-D target positions. This representation remains invariant under head and eye movements, and is a key component of sensory-motor systems for producing motor equivalent reaches to targets (Bullock, Grossberg, and Guenther, 1993).

Fuzzy ARTMAP, Slow Learning and Probability Estimation

A nonparametric probability estimation procedure using the fuzzy ARTMAP neural network is here described. Because the procedure does not make a priori assumptions about underlying probability distributions, it yields accurate estimates on a wide variety of prediction tasks. Fuzzy ARTMAP is used to perform probability estimation in two different modes. In a 'slow-learning' mode, input-output associations change slowly, with the strength of each association computing a conditional probability estimate. In 'max-nodes' mode, a fixed number of categories are coded during an initial fast learning interval, and weights are then tuned by slow learning. Simulations illustrate system performance on tasks in which various numbers of clusters in the set of input vectors mapped to a given class.