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Rob R. de Ruyter van Steveninck

Publications and source records attributed to Rob R. de Ruyter van Steveninck.

9 recordsLinked to original sources

Context dependent adaptation in a neural computation

Brains adapt to the statistical structure of their input. In the visual system, local light intensities change rapidly, the variance of the intensity changes more slowly, and the dynamic range of contrast itself changes more slowly still. We use a motion-sensitive neuron in the fly visual system to probe this hierarchy of adaptation phenomena, delivering naturalistic stimuli that have been simplified to have a clear separation of time scales. We show that the neural response to visual motion depends on contrast, and this dependence itself varies with context. Using the spike-triggered average velocity trajectory as a response measure, we find that context dependence is confined to a low-dimensional space, with a single dominant dimension. Across a wide range of conditions this adaptation serves to match the integration time to the mean interval between spikes, reducing redundancy.

q-bio.NC↗

The FlEye camera: Sampling the joint distribution of natural scenes and motion

To make efficient use of limited physical resources, the brain must match its coding and computational strategies to the statistical structure of input signals. An attractive testing ground for these principles is the problem of motion estimation in the fly visual system: we understand the optics of the compound eye, have a quantitative description of input signals and noise from the retina, and can record from output neurons that encode estimates of different velocity components. Furthermore, recent work provides a nearly complete wiring diagram of the intervening circuitry. What is missing is a characterization of the visual signals and motions that flies encounter in a natural context. We attack this directly with the development of a specialized camera that matches the high temporal resolution, optical properties, and spectral sensitivity of the fly's eye; inertial motion sensors provide ground truth about rotations and translations through the world. We describe the design, construction, and performance characteristics of this FlEye camera. To illustrate the opportunities created by this instrument we use data on movies and motion to construct optimal local motion estimators that can be compared with the responses of the fly's motion sensitive neurons.

q-bio.NC↗

The Neuron as a Direct Data-Driven Controller

In the quest to model neuronal function amidst gaps in physiological data, a promising strategy is to develop a normative theory that interprets neuronal physiology as optimizing a computational objective. This study extends the current normative models, which primarily optimize prediction, by conceptualizing neurons as optimal feedback controllers. We posit that neurons, especially those beyond early sensory areas, act as controllers, steering their environment towards a specific desired state through their output. This environment comprises both synaptically interlinked neurons and external motor sensory feedback loops, enabling neurons to evaluate the effectiveness of their control via synaptic feedback. Utilizing the novel Direct Data-Driven Control (DD-DC) framework, we model neurons as biologically feasible controllers which implicitly identify loop dynamics, infer latent states and optimize control. Our DD-DC neuron model explains various neurophysiological phenomena: the shift from potentiation to depression in Spike-Timing-Dependent Plasticity (STDP) with its asymmetry, the duration and adaptive nature of feedforward and feedback neuronal filters, the imprecision in spike generation under constant stimulation, and the characteristic operational variability and noise in the brain. Our model presents a significant departure from the traditional, feedforward, instant-response McCulloch-Pitts-Rosenblatt neuron, offering a novel and biologically-informed fundamental unit for constructing neural networks.

q-bio.NC↗

Optimal local estimates of visual motion in a natural environment

Many organisms, from flies to humans, use visual signals to estimate their motion through the world. To explore the motion estimation problem, we have constructed a camera/gyroscope system that allows us to sample, at high temporal resolution, the joint distribution of input images and rotational motions during a long walk in the woods. From these data we construct the optimal estimator of velocity based on spatial and temporal derivatives of image intensity in small patches of the visual world. Over the bulk of the naturally occurring dynamic range, the optimal estimator exhibits the same systematic errors seen in neural and behavioral responses, including the confounding of velocity and contrast. These results suggest that apparent errors of sensory processing may reflect an optimal response to the physical signals in the environment.

q-bio.NC↗

Efficient representation as a design principle for neural coding and computation

Does the brain construct an efficient representation of the sensory world? We review progress on this question, focusing on a series of experiments in the last decade which use fly vision as a model system in which theory and experiment can confront each other. Although the idea of efficient representation has been productive, clearly it is incomplete since it doesn't tell us which bits of sensory information are most valuable to the organism. We suggest that an organism which maximizes the (biologically meaningful) adaptive value of its actions given fixed resources should have internal representations of the outside world that are optimal in a very specific information theoretic sense: they maximize the information about the future of sensory inputs at a fixed value of the information about their past. This principle contains as special cases computations which the brain seems to carry out, and it should be possible to test this optimization directly. We return to the fly visual system and report the results of preliminary experiments that are in encouraging agreement with theory.

q-bio.NC↗

Neural coding of a natural stimulus ensemble: Uncovering information at sub-millisecond resolution

Our knowledge of the sensory world is encoded by neurons in sequences of discrete, identical pulses termed action potentials or spikes. There is persistent controversy about the extent to which the precise timing of these spikes is relevant to the function of the brain. We revisit this issue, using the motion-sensitive neurons of the fly visual system as a test case. New experimental methods allow us to deliver more nearly natural visual stimuli, comparable to those which flies encounter in free, acrobatic flight, and new mathematical methods allow us to draw more reliable conclusions about the information content of neural responses even when the set of possible responses is very large. We find that significant amounts of visual information are represented by details of the spike train at millisecond and sub-millisecond precision, even though the sensory input has a correlation time of ~60ms; different patterns of spike timing represent distinct motion trajectories, and the absolute timing of spikes points to particular features of these trajectories with high precision. Under these naturalistic conditions, the system continues to transmit more information at higher photon flux, even though individual photoreceptors are counting more than one million photons per second, and removes redundancy in the stimulus to generate a more efficient neural code.

q-bio.NC↗

Features and dimensions: Motion estimation in fly vision

We characterize the computation of motion in the fly visual system as a mapping from the high dimensional space of signals in the retinal photodetector array to the probability of generating an action potential in a motion sensitive neuron. Our approach to this problem identifies a low dimensional subspace of signals within which the neuron is most sensitive, and then samples this subspace to visualize the nonlinear structure of the mapping. The results illustrate the computational strategies predicted for a system that makes optimal motion estimates given the physical noise sources in the detector array. More generally, the hypothesis that neurons are sensitive to low dimensional subspaces of their inputs formalizes the intuitive notion of feature selectivity and suggests a strategy for characterizing the neural processing of complex, naturalistic sensory inputs.

q-bio.NC↗

Universality and individuality in a neural code

The problem of neural coding is to understand how sequences of action potentials (spikes) are related to sensory stimuli, motor outputs, or (ultimately) thoughts and intentions. One clear question is whether the same coding rules are used by different neurons, or by corresponding neurons in different individuals. We present a quantitative formulation of this problem using ideas from information theory, and apply this approach to the analysis of experiments in the fly visual system. We find significant individual differences in the structure of the code, particularly in the way that temporal patterns of spikes are used to convey information beyond that available from variations in spike rate. On the other hand, all the flies in our ensemble exhibit a high coding efficiency, so that every spike carries the same amount of information in all the individuals. Thus the neural code has a quantifiable mixture of individuality and universality.

physics.bio-ph↗

Entropy and Information in Neural Spike Trains

The nervous system represents time-dependent signals in sequences of discrete action potentials or spikes, all spikes are identical so that information is carried only in the spike arrival times. We show how to quantify this information, in bits, free from any assumptions about which features of the spike train or input waveform are most important. We apply this approach to the analysis of experiments on a motion-sensitive neuron in the fly visual system.

cond-mat↗