Action and behavior: a free-energy formulation

We have previously tried to explain perceptual inference and learning under a free-energy principle that pursues Helmholtz’s agenda to understand the brain in terms of energy minimization. It is fairly easy to show that making inferences about the causes of sensory data can be cast as the minimization of a free-energy bound on the likelihood of sensory inputs, given an internal model of how they were caused. In this article, we consider what would happen if the data themselves were sampled to minimize this bound. It transpires that the ensuing active sampling or inference is mandated by ergodic arguments based on the very existence of adaptive agents. Furthermore, it accounts for many aspects of motor behavior; from retinal stabilization to goal-seeking. In particular, it suggests that motor control can be understood as fulfilling prior expectations about proprioceptive sensations. This formulation can explain why adaptive behavior emerges in biological agents and suggests a simple alternative to optimal control theory. We illustrate these points using simulations of oculomotor control and then apply to same principles to cued and goal-directed movements. In short, the free-energy formulation may provide an alternative perspective on the motor control that places it in an intimate relationship with perception

Adaptive Real-Time Decoding of Brain Signals for Long-Term Control of a Neuro-Prosthetic Device

Changes in the statistical properties of neural signals recorded at the brain machine interface (BMI) pose significant challenges for accurate long-term control of prostheses interfaced directly with the brain by continuously altering the relationship between neural responses and desired action. In this thesis, we develop and test an adaptive decoding algorithm that can recover from changes in the statistical properties of neural signals within minutes. The adaptive decoding algorithm uses a Kalman filter as part of a dual-filter design to continuously optimize the relationship between the observed neural responses and the desired action of the prosthesis. Performance of the algorithm was evaluated by simulating the encoding of arm movement by neurons in the primary motor cortex under stationary conditions as well as nonstationary conditions depicting loss and/or replacement of neurons in the population. The time taken for the system to fully recover (3-12 minutes) was faster than other adaptive systems (Rotermund et al 2006) and resulted in errors that were well matched to the initial system performance. The algorithm adapts to the local properties of the stimulus and is able to decode movements with high accuracy outside the trained movement space. This implementation lends itself favorably toward a portable, robust long-term decoding approach at the brain machine interface capable of providing accurate real-time decoding of neural signals over periods of weeks to months without outside intervention

Adaptive coding for dynamic sensory inference

Behavior relies on the ability of sensory systems to infer properties of the environment from incoming stimuli. The accuracy of inference depends on the fidelity with which behaviorally relevant properties of stimuli are encoded in neural responses. High-fidelity encodings can be metabolically costly, but low-fidelity encodings can cause errors in inference. Here, we discuss general principles that underlie the tradeoff between encoding cost and inference error. We then derive adaptive encoding schemes that dynamically navigate this tradeoff. These optimal encodings tend to increase the fidelity of the neural representation following a change in the stimulus distribution, and reduce fidelity for stimuli that originate from a known distribution. We predict dynamical signatures of such encoding schemes and demonstrate how known phenomena, such as burst coding and firing rate adaptation, can be understood as hallmarks of optimal coding for accurate inference

Attentional Enhancement of Auditory Mismatch Responses: a DCM/MEG Study.

Despite similar behavioral effects, attention and expectation influence evoked responses differently: Attention typically enhances event-related responses, whereas expectation reduces them. This dissociation has been reconciled under predictive coding, where prediction errors are weighted by precision associated with attentional modulation. Here, we tested the predictive coding account of attention and expectation using magnetoencephalography and modeling. Temporal attention and sensory expectation were orthogonally manipulated in an auditory mismatch paradigm, revealing opposing effects on evoked response amplitude. Mismatch negativity (MMN) was enhanced by attention, speaking against its supposedly pre-attentive nature. This interaction effect was modeled in a canonical microcircuit using dynamic causal modeling, comparing models with modulation of extrinsic and intrinsic connectivity at different levels of the auditory hierarchy. While MMN was explained by recursive interplay of sensory predictions and prediction errors, attention was linked to the gain of inhibitory interneurons, consistent with its modulation of sensory precision

Free-energy and the brain

If one formulates Helmholtz's ideas about perception in terms of modern-day theories one arrives at a model of perceptual inference and learning that can explain a remarkable range of neurobiological facts. Using constructs from statistical physics it can be shown that the problems of inferring what cause our sensory input and learning causal regularities in the sensorium can be resolved using exactly the same principles. Furthermore, inference and learning can proceed in a biologically plausible fashion. The ensuing scheme rests on Empirical Bayes and hierarchical models of how sensory information is generated. The use of hierarchical models enables the brain to construct prior expectations in a dynamic and context-sensitive fashion. This scheme provides a principled way to understand many aspects of the brain's organisation and responses.In this paper, we suggest that these perceptual processes are just one emergent property of systems that conform to a free-energy principle. The free-energy considered here represents a bound on the surprise inherent in any exchange with the environment, under expectations encoded by its state or configuration. A system can minimise free-energy by changing its configuration to change the way it samples the environment, or to change its expectations. These changes correspond to action and perception respectively and lead to an adaptive exchange with the environment that is characteristic of biological systems. This treatment implies that the system's state and structure encode an implicit and probabilistic model of the environment. We will look at models entailed by the brain and how minimisation of free-energy can explain its dynamics and structure

Population decoding in rat barrel cortex: optimizing the linear readout of correlated population responses

Sensory information is encoded in the response of neuronal populations. How might this information be decoded by downstream neurons? Here we analyzed the responses of simultaneously recorded barrel cortex neurons to sinusoidal vibrations of varying amplitudes preceded by three adapting stimuli of 0, 6 and 12 µm in amplitude. Using the framework of signal detection theory, we quantified the performance of a linear decoder which sums the responses of neurons after applying an optimum set of weights. Optimum weights were found by the analytical solution that maximized the average signal-to-noise ratio based on Fisher linear discriminant analysis. This provided a biologically plausible decoder that took into account the neuronal variability, covariability, and signal correlations. The optimal decoder achieved consistent improvement in discrimination performance over simple pooling. Decorrelating neuronal responses by trial shuffling revealed that, unlike pooling, the performance of the optimal decoder was minimally affected by noise correlation. In the non-adapted state, noise correlation enhanced the performance of the optimal decoder for some populations. Under adaptation, however, noise correlation always degraded the performance of the optimal decoder. Nonetheless, sensory adaptation improved the performance of the optimal decoder mainly by increasing signal correlation more than noise correlation. Adaptation induced little systematic change in the relative direction of signal and noise. Thus, a decoder which was optimized under the non-adapted state generalized well across states of adaptation

Hierarchical Modular Optimization of Convolutional Networks Achieves Representations Similar to Macaque IT and Human Ventral Stream

Humans recognize visually-presented objects rapidly and accurately. To understand this ability, we seek to construct models of the ventral stream, the series of cortical areas thought to subserve object recognition. One tool to assess the quality of a model of the ventral stream is the Representational Dissimilarity Matrix (RDM), which uses a set of visual stimuli and measures the distances produced in either the brain (i.e. fMRI voxel responses, neural firing rates) or in models (fea-ures). Previous work has shown that all known models of the ventral stream fail to capture the RDM pattern observed in either IT cortex, the highest ventral area, or in the human ventral stream. In this work, we construct models of the ventral stream using a novel optimization procedure for category-level object recognition problems, and produce RDMs resembling both macaque IT and human ventral stream. The model, while novel in the optimization procedure, further develops a long-standing functional hypothesis that the ventral visual stream is a hierarchically arranged series of processing stages optimized for visual object recognition