Fixational Instability and Natural Image Statistics: Implications for Early Visual Representations

Under natural viewing conditions small movements of the eye, head, and body prevent the maintenance of a steady direction of gaze. It is known that stimuli tend to fade when they a restabilized on the retina for several seconds. However; it is unclear whether the physiological motion of the retinal image serves a visual purpose during the brief periods of natural visual fixation. This study examines the impact of fixational instability on the statistics of the visua1 input to the retina and on the structure of neural activity in the early visual system. We show that fixational instability introduces a component in the retinal input signals that in the presence of natural images, lacks spatial correlations. This component strongly influences neural activity in a model of the LGN. It decorrelates cell responses even if the contrast sensitivity functions of simulated cells arc not perfectly tuned to counterbalance the power-law spectrum of natural images. A decorrelation of neural activity at the early stages of the visual system has been proposed to be beneficial for discarding statistical redundancies in the input signals. The results of this study suggest that fixational instability might contribute to establishing efficient representations of natural stimuli.

Self-Organizing Information Fusion and Hierarchical Knowledge Discovery: A New Framework Using Artmap Neural Networks

Classifying novel terrain or objects from sparse, complex data may require the resolution of conflicting information from sensors woring at different times, locations, and scales, and from sources with different goals and situations. Information fusion methods can help resolve inconsistencies, as when eveidence variously suggests that and object's class is car, truck, or airplane. The methods described her address a complementary problem, supposing that information from sensors and experts is reliable though inconsistent, as when evidence suggests that an object's class is car, vehicle, and man-made. Underlying relationships among classes are assumed to be unknown to the autonomated system or the human user. The ARTMAP information fusion system uses distributed code representations that exploit the neural network's capacity for one-to-many learning in order to produce self-organizing expert systems that discover hierachical knowlege structures. The fusion system infers multi-level relationships among groups of output classes, without any supervised labeling of these relationships. The procedure is illustrated with two image examples, but is not limited to image domain.

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)

Neural Network and Bioinformatic Methods for Predicting HIV-1 Protease Inhibitor Resistance

This article presents a new method for predicting viral resistance to seven protease inhibitors from the HIV-1 genotype, and for identifying the positions in the protease gene at which the specific nature of the mutation affects resistance. The neural network Analog ARTMAP predicts protease inhibitor resistance from viral genotypes. A feature selection method detects genetic positions that contribute to resistance both alone and through interactions with other positions. This method has identified positions 35, 37, 62, and 77, where traditional feature selection methods have not detected a contribution to resistance. At several positions in the protease gene, mutations confer differing degress of resistance, depending on the specific amino acid to which the sequence has mutated. To find these positions, an Amino Acid Space is introduced to represent genes in a vector space that captures the functional similarity between amino acid pairs. Feature selection identifies several new positions, including 36, 37, and 43, with amino acid-specific contributions to resistance. Analog ARTMAP networks applied to inputs that represent specific amino acids at these positions perform better than networks that use only mutation locations.

A Dopamine-Acetylcholine Cascade: Simulating Learned and Lesion-Induced Behavior ff Striatal Cholinergic Interneurons

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 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, probably mediated by GABAergic NOS interneurons, exceeds a threshold, its effect is amplified by a KIR current to generate a prolongued 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.

A Neural Model of Visually Guided Steering, Obstacle Avoidance, and Route Selection

A neural model is developed to explain how humans can approach a goal object on foot while steering around obstacles to avoid collisions in a cluttered environment. The model uses optic flow from a 3D virtual reality environment to determine the position of objects based on motion discotinuities, and computes heading direction, or the direction of self-motion, from global optic flow. The cortical representation of heading interacts with the representations of a goal and obstacles such that the goal acts as an attractor of heading, while obstacles act as repellers. In addition the model maintains fixation on the goal object by generating smooth pursuit eye movements. Eye rotations can distort the optic flow field, complicating heading perception, and the model uses extraretinal signals to correct for this distortion and accurately represent heading. The model explains how motion processing mechanisms in cortical areas MT, MST, and VIP can be used to guide steering. The model quantitatively simulates human psychophysical data about visually-guided steering, obstacle avoidance, and route selection.

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)

A Local Circuit Model of Learned Straitial and Dopamine Cell Responses under Probabilistic Schedules of Reward

Before choosing, it helps to know both the expected value signaled by a predictive cue and the associated uncertainty that the reward will be forthcoming. Recently, Fiorillo et al. (2003) found the dopamine (DA) neurons of the SNc exhibit sustained responses related to the uncertainty that a cure will be followed by reward, in addition to phasic responses related to reward prediction errors (RPEs). This suggests that cue-dependent anticipations of the timing, magnitude, and uncertainty of rewards are learned and reflected in components of the DA signals broadcast by SNc neurons. What is the minimal local circuit model that can explain such multifaceted reward-related learning? A new computational model shows how learned uncertainty responses emerge robustly on single trial along with phasic RPE responses, such that both types of DA responses exhibit the empirically observed dependence on conditional probability, expected value of reward, and time since onset of the reward-predicting cue. The model includes three major pathways for computing: immediate expected values of cures, timed predictions of reward magnitudes (and RPEs), and the uncertainty associated with these predictions. The first two model pathways refine those previously modeled by Brown et al. (1999). A third, newly modeled, pathway is formed by medium spiny projection neurons (MSPNs) of the matrix compartment of the striatum, whose axons co-release GABA and a neuropeptide, substance P, both at synapses with GABAergic neurons in the SNr and with the dendrites (in SNr) of DA neurons whose somas are in ventral SNc. Co-release enables efficient computation of sustained DA uncertainty responses that are a non-monotonic function of the conditonal probability that a reward will follow the cue. The new model's incorporation of a striatal microcircuit allowed it to reveals that variability in striatal cholinergic transmission can explain observed difference, between monkeys, in the amplitutude of the non-monotonic uncertainty function. Involvement of matriceal MSPNs and striatal cholinergic transmission implpies a relation between uncertainty in the cue-reward contigency and action-selection functions of the basal ganglia. The model synthesizes anatomical, electrophysiological and behavioral data regarding the midbrain DA system in a novel way, by relating the ability to compute uncertainty, in parallel with other aspects of reward contingencies, to the unique distribution of SP inputs in ventral SN.

Neural Models of Motion Integration, Segmentation, and Probablistic Decision-Making

When brain mechanism carry out motion integration and segmentation processes that compute unambiguous global motion percepts from ambiguous local motion signals? Consider, for example, a deer running at variable speeds behind forest cover. The forest cover is an occluder that creates apertures through which fragments of the deer's motion signals are intermittently experienced. The brain coherently groups these fragments into a trackable percept of the deer in its trajectory. Form and motion processes are needed to accomplish this using feedforward and feedback interactions both within and across cortical processing streams. All the cortical areas V1, V2, MT, and MST are involved in these interactions. Figure-ground processes in the form stream through V2, such as the seperation of occluding boundaries of the forest cover from the boundaries of the deer, select the motion signals which determine global object motion percepts in the motion stream through MT. Sparse, but unambiguous, feauture tracking signals are amplified before they propogate across position and are intergrated with far more numerous ambiguous motion signals. Figure-ground and integration processes together determine the global percept. A neural model predicts the processing stages that embody these form and motion interactions. Model concepts and data are summarized about motion grouping across apertures in response to a wide variety of displays, and probabilistic decision making in parietal cortex in response to random dot displays.

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.

Neural Dynamics of Saccadic and Smooth Pursuit Eye Movement Coordination during Visual Tracking of Unpredictably Moving Targets

How does the brain use eye movements to track objects that move in unpredictable directions and speeds? Saccadic eye movements rapidly foveate peripheral visual or auditory targets and smooth pursuit eye movements keep the fovea pointed toward an attended moving target. Analyses of tracking data in monkeys and humans reveal systematic deviations from predictions of the simplest model of saccade-pursuit interactions, which would use no interactions other than common target selection and recruitment of shared motoneurons. Instead, saccadic and smooth pursuit movements cooperate to cancel errors of gaze position and velocity, and thus to maximize target visibility through time. How are these two systems coordinated to promote visual localization and identification of moving targets? How are saccades calibrated to correctly foveate a target despite its continued motion during the saccade? A neural model proposes answers to such questions. The modeled interactions encompass motion processing areas MT, MST, FPA, DLPN and NRTP; saccade planning and execution areas FEF and SC; the saccadic generator in the brain stem; and the cerebellum. Simulations illustrate the model’s ability to functionally explain and quantitatively simulate anatomical, neurophysiological and behavioral data about SAC-SPEM tracking.

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.

Dopaminergic and Non-Dopaminergic Value Systems in Conditioning and Outcome-Specific Revaluation

Animals are motivated to choose environmental options that can best satisfy current needs. To explain such choices, this paper introduces the MOTIVATOR (Matching Objects To Internal Values Triggers Option Revaluations) neural model. MOTIVATOR describes cognitiveemotional interactions between higher-order sensory cortices and an evaluative neuraxis composed of the hypothalamus, amygdala, and orbitofrontal cortex. Given a conditioned stimulus (CS), the model amygdala and lateral hypothalamus interact to calculate the expected current value of the subjective outcome that the CS predicts, constrained by the current state of deprivation or satiation. The amygdala relays the expected value information to orbitofrontal cells that receive inputs from anterior inferotemporal cells, and medial orbitofrontal cells that receive inputs from rhinal cortex. The activations of these orbitofrontal cells code the subjective values of objects. These values guide behavioral choices. The model basal ganglia detect errors in CS-specific predictions of the value and timing of rewards. Excitatory inputs from the pedunculopontine nucleus interact with timed inhibitory inputs from model striosomes in the ventral striatum to regulate dopamine burst and dip responses from cells in the substantia nigra pars compacta and ventral tegmental area. Learning in cortical and striatal regions is strongly modulated by dopamine. The model is used to address tasks that examine food-specific satiety, Pavlovian conditioning, reinforcer devaluation, and simultaneous visual discrimination. Model simulations successfully reproduce discharge dynamics of known cell types, including signals that predict saccadic reaction times and CS-dependent changes in systolic blood pressure.

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.

Exact Geosedics and Shortest Paths on Polyhedral Surface

We present two algorithms for computing distances along a non-convex polyhedral surface. The first algorithm computes exact minimal-geodesic distances and the second algorithm combines these distances to compute exact shortest-path distances along the surface. Both algorithms have been extended to compute the exact minimalgeodesic paths and shortest paths. These algorithms have been implemented and validated on surfaces for which the correct solutions are known, in order to verify the accuracy and to measure the run-time performance, which is cubic or less for each algorithm. The exact-distance computations carried out by these algorithms are feasible for large-scale surfaces containing tens of thousands of vertices, and are a necessary component of near-isometric surface flattening methods that accurately transform curved manifolds into flat representations.