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Summary: A central goal in sensory neuroscience is to fully characterize a neuron''s input-output relation. However, strong nonlinearities in the responses of sensory neurons have made it difficult to develop models that generalize to arbitrary stimuli. Typically, the standard linear-nonlinear models break down when neurons exhibit stimulus-dependent modulations of their gain or selectivity. We studied these issues in optic-flow processing neurons in the fly. We found that the neurons'' receptive fields are fully described by a time-varying vector field that is space-time separable. Increasing the stimulus strength, however, strongly reduces the neurons'' gain and selectivity. To capture these changes in response behavior, we extended the linear-nonlinear model by a biophysically motivated gain and selectivity mechanism. We fit all model parameters directly to the data and show that the model now characterizes the neurons'' input-output relation well over the full range of motion stimuli. [Copyright &y& Elsevier]

Summary: According to Barlow’s seminal “efficient coding hypothesis,” the coding strategy of sensory neurons should be matched to the statistics of stimuli that occur in an animal’s natural habitat. Using an automatic search technique, we here test this hypothesis and identify stimulus ensembles that sensory neurons are optimized for. Focusing on grasshopper auditory receptor neurons, we find that their optimal stimulus ensembles differ from the natural environment, but largely overlap with a behaviorally important sub-ensemble of the natural sounds. This indicates that the receptors are optimized for peak rather than average performance. More generally, our results suggest that the coding strategies of sensory neurons are heavily influenced by differences in behavioral relevance among natural stimuli. [Copyright &y& Elsevier]

In many brain areas, neuronal activity is associated with a variety of behavioral and environmental variables. In particular, neuronal responses in the zebrafish hindbrain relate to oculomotor and swimming variables as well as sensory information. However, the precise functional organization of the neurons has been difficult to unravel because neuronal responses are heterogeneous. Here, we used dimensionality reduction methods on neuronal population data to reveal the role of the hindbrain in visually driven oculomotor behavior and swimming. We imaged neuronal activity in zebrafish expressing GCaMP6s in the nucleus of almost all neurons while monitoring the behavioral response to gratings that rotated with different speeds. We then used reduced-rank regression, a method that condenses the sensory and motor variables into a smaller number of "features," to predict the fluorescence traces of all ROIs (regions of interest). Despite the potential complexity of the visuo-motor transformation, our analysis revealed that a large fraction of the population activity can be explained by only two features. Based on the contribution of these features to each ROI's activity, ROIs formed three clusters. One cluster was related to vergent movements and swimming, whereas the other two clusters related to leftward and rightward rotation. Voxels corresponding to these clusters were segregated anatomically, with leftward and rightward rotation clusters located selectively to the left and right hemispheres, respectively. Just as described in many cortical areas, our analysis revealed that single-neuron complexity co-exists with a simpler population-level description, thereby providing insights into the organization of visuo-motor transformations in the hindbrain. [Display omitted] • Bilaterally independent visual stimuli decouple eye movements and elicit swimming • In the dorsal hindbrain, activity related to the eyes and tail is low dimensional • Neurons form clusters related to vergent and left/right rotational movements • Rotation and vergence clusters have distinct anatomical organization Feierstein et al. use visual stimuli that elicit decoupled eye movements and swimming in zebrafish larvae. Combining regression and dimensionality reduction techniques, they show that behavior-related activity in the hindbrain is low dimensional. Neurons form functional and spatial clusters related to vergent and rotational movements. [ABSTRACT FROM AUTHOR]

Summary Most brain functions involve interactions among multiple, distinct areas or nuclei. For instance, visual processing in primates requires the appropriate relaying of signals across many distinct cortical areas. Yet our understanding of how populations of neurons in interconnected brain areas communicate is in its infancy. Here we investigate how trial-to-trial fluctuations of population responses in primary visual cortex (V1) are related to simultaneously recorded population responses in area V2. Using dimensionality reduction methods, we find that V1-V2 interactions occur through a communication subspace: V2 fluctuations are related to a small subset of V1 population activity patterns, distinct from the largest fluctuations shared among neurons within V1. In contrast, interactions between subpopulations within V1 are less selective. We propose that the communication subspace may be a general, population-level mechanism by which activity can be selectively routed across brain areas. Highlights • Visual cortical areas interact through a communication subspace (CS) • The CS defines which activity patterns in a source area relate to downstream activity • The largest activity patterns in a source area are not matched to the CS • The CS allows for selective and flexible routing of population signals between areas Most brain functions require the selective and flexible routing of neuronal activity between cortical areas. Using paired population recordings from multiple visual cortical areas, Semedo et al. find a population-level mechanism that can achieve this routing, termed a communication subspace. [ABSTRACT FROM AUTHOR]

Summary Dopamine neurons encode the difference between actual and predicted reward, or reward prediction error (RPE). Although many models have been proposed to account for this computation, it has been difficult to test these models experimentally. Here we established an awake electrophysiological recording system, combined with rabies virus and optogenetic cell-type identification, to characterize the firing patterns of monosynaptic inputs to dopamine neurons while mice performed classical conditioning tasks. We found that each variable required to compute RPE, including actual and predicted reward, was distributed in input neurons in multiple brain areas. Further, many input neurons across brain areas signaled combinations of these variables. These results demonstrate that even simple arithmetic computations such as RPE are not localized in specific brain areas but, rather, distributed across multiple nodes in a brain-wide network. Our systematic method to examine both activity and connectivity revealed unexpected redundancy for a simple computation in the brain. [ABSTRACT FROM AUTHOR]

Lateral intraparietal (LIP) neurons represent formation of perceptual decisions involving eye movements. In circuit models for these decisions, neural ensembles that encode actions compete to form decisions. Consequently, representation and readout of the decision variables (DVs) are implemented similarly for decisions with identical competing actions, irrespective of input and task context differences. Further, DVs are encoded as partially potentiated action plans through balance of activity of action-selective ensembles. Here, we test those core principles. We show that in a novel face-discrimination task, LIP firing rates decrease with supporting evidence, contrary to conventional motion-discrimination tasks. These opposite response patterns arise from similar mechanisms in which decisions form along curved population-response manifolds misaligned with action representations. These manifolds rotate in state space based on context, indicating distinct optimal readouts for different tasks. We show similar manifolds in lateral and medial prefrontal cortices, suggesting similar representational geometry across decision-making circuits. [Display omitted] • We examine parietal neural activity in motion and face discrimination tasks • Population neural response dynamics form a curved manifold during decision-making • Manifolds rotates across tasks, changing optimal readout of the decision variable • Circuit models of perceptual decisions need revision to include task dependency Comparison of neuronal activity during decision-making in face and motion discrimination tasks reveals task-dependent response geometry that shapes optimal readout of the decision variable. [ABSTRACT FROM AUTHOR]