Perceptual inference predicts contextual modulations of sensory responses.

Sensory receptive fields (RFs) vary as a function of stimulus properties and measurement methods. Previous stimuli or surrounding stimuli facilitate, suppress, or change the selectivity of sensory neurons' responses. Here, we propose that these spatiotemporal contextual dependencies are signatures of efficient perceptual inference and can be explained by a single neural mechanism, input targeted divisive inhibition. To respond both selectively and reliably, sensory neurons should behave as active predictors rather than passive filters. In particular, they should remove input they can predict ("explain away") from the synaptic inputs to all other neurons. This implies that RFs are constantly and dynamically reshaped by the spatial and temporal context, while the true selectivity of sensory neurons resides in their "predictive field." This approach motivates a reinvestigation of sensory representations and particularly the role and specificity of surround suppression and adaptation in sensory areas.

Construction of direction selectivity through local energy computations in primary visual cortex.

Despite detailed knowledge about the anatomy and physiology of neurons in primary visual cortex (V1), the large numbers of inputs onto a given V1 neuron make it difficult to relate them to the neuron's functional properties. For example, models of direction selectivity (DS), such as the Energy Model, can successfully describe the computation of phase-invariant DS at a conceptual level, while leaving it unclear how such computations are implemented by cortical circuits. Here, we use statistical modeling to derive a description of DS computation for both simple and complex cells, based on physiologically plausible operations on their inputs. We present a new method that infers the selectivity of a neuron's inputs using extracellular recordings in macaque in the context of random bar stimuli and natural movies in cat. Our results suggest that DS is initially constructed in V1 simple cells through summation and thresholding of non-DS inputs with appropriate spatiotemporal relationships. However, this de novo construction of DS is rare, and a majority of DS simple cells, and all complex cells, appear to receive both excitatory and suppressive inputs that are already DS. For complex cells, these numerous DS inputs typically span a fraction of their overall receptive fields and have similar spatiotemporal tuning but different phase and spatial positions, suggesting an elaboration to the Energy Model that incorporates spatially localized computation. Furthermore, we demonstrate how these computations might be constructed from biologically realizable components, and describe a statistical model consistent with the feed-forward framework suggested by Hubel and Wiesel.

Neural processing as causal inference.

Perception is about making sense, that is, understanding what events in the outside world caused the sensory observations. Consistent with this intuition, many aspects of human behavior confronting noise and ambiguity are well explained by principles of causal inference. Extending these insights, recent studies have applied the same powerful set of tools to perceptual processing at the neural level. According to these approaches, microscopic neural structures solve elementary probabilistic tasks and can be combined to construct hierarchical predictive models of the sensory input. This framework suggests that variability in neural responses reflects the inherent uncertainty associated with sensory interpretations and that sensory neurons are active predictors rather than passive filters of their inputs. Causal inference can account parsimoniously and quantitatively for non-linear dynamical properties in single synapses, single neurons and sensory receptive fields.