Learning selective top-down control enhances performance in a visual categorization task.

We model the putative neuronal and synaptic mechanisms involved in learning a visual categorization task, taking inspiration from single-cell recordings in inferior temporal cortex (ITC). Our working hypothesis is that learning the categorization task involves both bottom-up, ITC to prefrontal cortex (PFC), and top-down (PFC to ITC) synaptic plasticity and that the latter enhances the selectivity of the ITC neurons encoding the task-relevant features of the stimuli, thereby improving the signal-to-noise ratio. We test this hypothesis by modeling both areas and their connections with spiking neurons and plastic synapses, ITC acting as a feature-selective layer and PFC as a category coding layer. This minimal model gives interesting clues as to properties and function of the selective feedback signal from PFC to ITC that help solving a categorization task. In particular, we show that, when the stimuli are very noisy because of a large number of nonrelevant features, the feedback structure helps getting better categorization performance and decreasing the reaction time. It also affects the speed and stability of the learning process and sharpens tuning curves of ITC neurons. Furthermore, the model predicts a modulation of neural activities during error trials, by which the differential selectivity of ITC neurons to task-relevant and task-irrelevant features diminishes or is even reversed, and modulations in the time course of neural activities that appear when, after learning, corrupted versions of the stimuli are input to the network

Beta oscillations underlie top-down, feedback control while gamma oscillations reflect bottom-up, feedforward influences

Prefrontal cortex (PFC) is critical to behavioral flexibility and, hence, the top-down control over bottom-up sensory information. The mechanisms underlying this capacity have been hypothesized to involve the propagation of alpha/beta (8-30 Hz) oscillations via feedback connections to sensory regions. In contrast, gamma (30-160 Hz) oscillations are thought to arise as a function of bottom-up, feedforward stimulation. To test the hypothesis that such oscillatory phenomena embody such functional roles, we assessed the performance of nine monkeys on tasks of learning, categorization, and working memory concurrent with recording of local field potentials (LFPs) from PFC. The first set of tasks consisted of two classes of learning: one, explicit and, another, implicit. Explicit learning is a conscious process that demands top-down control, and in these tasks alpha/beta oscillations tracked learning. In contrast, implicit learning is an unconscious process that is automatic (i.e. bottom up), and in this task alpha/beta oscillations did not track learning. We next looked at dot-pattern categorization. In this task, category exemplars were generated by jittering the dot locations of a prototype. By chance, some of these exemplars were similar to the prototype (low distortion), and others were not (high distortion). Behaviorally, the monkeys performed well on both distortion levels. However, alpha/beta band oscillations carried more category information at high distortions, while gamma-band category information was greatest on low distortions. Overall, the greater the need for top-down control (i.e. high distortion), the greater the beta, and the lesser the need (i.e. low distortion), the greater the gamma. Finally, laminar electrodes were used to record from animals trained on working memory tasks. Each laminar probe was lowered so that its set of contacts sampled all cortical layers. During these tasks, gamma oscillations peaked in superficial layers, while alpha/beta peaked in deep layers. Moreover, these deep-layer alpha/beta oscillations entrained superficial alpha/beta, and modulated the amplitude of superficial-layer gamma oscillations. These laminar distinctions are consistent with anatomy: feedback neurons originate in deep layers and feedforward neurons in superficial layers. In summary, alpha/beta oscillations reflect top-down control and feedback connectivity, while gamma oscillations reflect bottom-up processes and feedforward connectivity

A Neural Model for Self Organizing Feature Detectors and Classifiers in a Network Hierarchy

Many models of early cortical processing have shown how local learning rules can produce efficient, sparse-distributed codes in which nodes have responses that are statistically independent and low probability. However, it is not known how to develop a useful hierarchical representation, containing sparse-distributed codes at each level of the hierarchy, that incorporates predictive feedback from the environment. We take a step in that direction by proposing a biologically plausible neural network model that develops receptive fields, and learns to make class predictions, with or without the help of environmental feedback. The model is a new type of predictive adaptive resonance theory network called Receptive Field ARTMAP, or RAM. RAM self organizes internal category nodes that are tuned to activity distributions in topographic input maps. Each receptive field is composed of multiple weight fields that are adapted via local, on-line learning, to form smooth receptive ftelds that reflect; the statistics of the activity distributions in the input maps. When RAM generates incorrect predictions, its vigilance is raised, amplifying subtractive inhibition and sharpening receptive fields until the error is corrected. Evaluation on several classification benchmarks shows that RAM outperforms a related (but neurally implausible) model called Gaussian ARTMAP, as well as several standard neural network and statistical classifters. A topographic version of RAM is proposed, which is capable of self organizing hierarchical representations. Topographic RAM is a model for receptive field development at any level of the cortical hierarchy, and provides explanations for a variety of perceptual learning data.Defense Advanced Research Projects Agency and Office of Naval Research (N00014-95-1-0409

The Cat Is On the Mat. Or Is It a Dog? Dynamic Competition in Perceptual Decision Making

Recent neurobiological findings suggest that the brain solves simple perceptual decision-making tasks by means of a dynamic competition in which evidence is accumulated in favor of the alternatives. However, it is unclear if and how the same process applies in more complex, real-world tasks, such as the categorization of ambiguous visual scenes and what elements are considered as evidence in this case. Furthermore, dynamic decision models typically consider evidence accumulation as a passive process disregarding the role of active perception strategies. In this paper, we adopt the principles of dynamic competition and active vision for the realization of a biologically- motivated computational model, which we test in a visual catego- rization task. Moreover, our system uses predictive power of the features as the main dimension for both evidence accumulation and the guidance of active vision. Comparison of human and synthetic data in a common experimental setup suggests that the proposed model captures essential aspects of how the brain solves perceptual ambiguities in time. Our results point to the importance of the proposed principles of dynamic competi- tion, parallel specification, and selection of multiple alternatives through prediction, as well as active guidance of perceptual strategies for perceptual decision-making and the resolution of perceptual ambiguities. These principles could apply to both the simple perceptual decision problems studied in neuroscience and the more complex ones addressed by vision research.Peer reviewe

The hippocampus and cerebellum in adaptively timed learning, recognition, and movement

The concepts of declarative memory and procedural memory have been used to distinguish two basic types of learning. A neural network model suggests how such memory processes work together as recognition learning, reinforcement learning, and sensory-motor learning take place during adaptive behaviors. To coordinate these processes, the hippocampal formation and cerebellum each contain circuits that learn to adaptively time their outputs. Within the model, hippocampal timing helps to maintain attention on motivationally salient goal objects during variable task-related delays, and cerebellar timing controls the release of conditioned responses. This property is part of the model's description of how cognitive-emotional interactions focus attention on motivationally valued cues, and how this process breaks down due to hippocampal ablation. The model suggests that the hippocampal mechanisms that help to rapidly draw attention to salient cues could prematurely release motor commands were not the release of these commands adaptively timed by the cerebellum. The model hippocampal system modulates cortical recognition learning without actually encoding the representational information that the cortex encodes. These properties avoid the difficulties faced by several models that propose a direct hippocampal role in recognition learning. Learning within the model hippocampal system controls adaptive timing and spatial orientation. Model properties hereby clarify how hippocampal ablations cause amnesic symptoms and difficulties with tasks which combine task delays, novelty detection, and attention towards goal objects amid distractions. When these model recognition, reinforcement, sensory-motor, and timing processes work together, they suggest how the brain can accomplish conditioning of multiple sensory events to delayed rewards, as during serial compound conditioning.Air Force Office of Scientific Research (F49620-92-J-0225, F49620-86-C-0037, 90-0128); Advanced Research Projects Agency (ONR N00014-92-J-4015); Office of Naval Research (N00014-91-J-4100, N00014-92-J-1309, N00014-92-J-1904); National Institute of Mental Health (MH-42900

Acetylcholine neuromodulation in normal and abnormal learning and memory: vigilance control in waking, sleep, autism, amnesia, and Alzheimer's disease

This article provides a unified mechanistic neural explanation of how learning, recognition, and cognition break down during Alzheimer's disease, medial temporal amnesia, and autism. It also clarifies whey there are often sleep disturbances during these disorders. A key mechanism is how acetylcholine modules vigilance control in cortical layer

Learning to become an expert : reinforcement learning and the acquisition of perceptual expertise

To elucidate the neural mechanisms underlying the development of perceptual expertise, we recorded ERPs while participants performed a categorization task. We found that as participants learned to discriminate computer-generated "blob'' stimuli, feedback modulated the amplitude of the errorrelated negativity (ERN)-an ERP component thought to reflect error evaluation within medial-frontal cortex. As participants improved at the categorization task, we also observed an increase in amplitude of an ERP component associated with object recognition (the N250). The increase in N250 amplitude preceded an increase in amplitude of an ERN component associated with internal error evaluation (the response ERN). Importantly, these electroencephalographic changes were not observed for participants who failed to improve on the categorization task. Our results suggest that the acquisition of perceptual expertise relies on interactions between the posterior perceptual system and the reinforcement learning system involving medial-frontal cortex

Adaptive Resonance Theory: Self-Organizing Networks for Stable Learning, Recognition, and Prediction

Adaptive Resonance Theory (ART) is a neural theory of human and primate information processing and of adaptive pattern recognition and prediction for technology. Biological applications to attentive learning of visual recognition categories by inferotemporal cortex and hippocampal system, medial temporal amnesia, corticogeniculate synchronization, auditory streaming, speech recognition, and eye movement control are noted. ARTMAP systems for technology integrate neural networks, fuzzy logic, and expert production systems to carry out both unsupervised and supervised learning. Fast and slow learning are both stable response to large non stationary databases. Match tracking search conjointly maximizes learned compression while minimizing predictive error. Spatial and temporal evidence accumulation improve accuracy in 3-D object recognition. Other applications are noted.Office of Naval Research (N00014-95-I-0657, N00014-95-1-0409, N00014-92-J-1309, N00014-92-J4015); National Science Foundation (IRI-94-1659