Closed-loop estimation of retinal network sensitivity reveals signature of efficient coding

According to the theory of efficient coding, sensory systems are adapted to represent natural scenes with high fidelity and at minimal metabolic cost. Testing this hypothesis for sensory structures performing non-linear computations on high dimensional stimuli is still an open challenge. Here we develop a method to characterize the sensitivity of the retinal network to perturbations of a stimulus. Using closed-loop experiments, we explore selectively the space of possible perturbations around a given stimulus. We then show that the response of the retinal population to these small perturbations can be described by a local linear model. Using this model, we computed the sensitivity of the neural response to arbitrary temporal perturbations of the stimulus, and found a peak in the sensitivity as a function of the frequency of the perturbations. Based on a minimal theory of sensory processing, we argue that this peak is set to maximize information transmission. Our approach is relevant to testing the efficient coding hypothesis locally in any context where no reliable encoding model is known

Detecting and Estimating Signals over Noisy and Unreliable Synapses: Information-Theoretic Analysis

The temporal precision with which neurons respond to synaptic inputs has a direct bearing on the nature of the neural code. A characterization of the neuronal noise sources associated with different sub-cellular components (synapse, dendrite, soma, axon, and so on) is needed to understand the relationship between noise and information transfer. Here we study the effect of the unreliable, probabilistic nature of synaptic transmission on information transfer in the absence of interaction among presynaptic inputs. We derive theoretical lower bounds on the capacity of a simple model of a cortical synapse under two different paradigms. In signal estimation, the signal is assumed to be encoded in the mean firing rate of the presynaptic neuron, and the objective is to estimate the continuous input signal from the postsynaptic voltage. In signal detection, the input is binary, and the presence or absence of a presynaptic action potential is to be detected from the postsynaptic voltage. The efficacy of information transfer in synaptic transmission is characterized by deriving optimal strategies under these two paradigms. On the basis of parameter values derived from neocortex, we find that single cortical synapses cannot transmit information reliably, but redundancy obtained using a small number of multiple synapses leads to a significant improvement in the information capacity of synaptic transmission

How behavioral constraints may determine optimal sensory representations

The sensory-triggered activity of a neuron is typically characterized in terms of a tuning curve, which describes the neuron's average response as a function of a parameter that characterizes a physical stimulus. What determines the shapes of tuning curves in a neuronal population? Previous theoretical studies and related experiments suggest that many response characteristics of sensory neurons are optimal for encoding stimulus-related information. This notion, however, does not explain the two general types of tuning profiles that are commonly observed: unimodal and monotonic. Here, I quantify the efficacy of a set of tuning curves according to the possible downstream motor responses that can be constructed from them. Curves that are optimal in this sense may have monotonic or non-monotonic profiles, where the proportion of monotonic curves and the optimal tuning curve width depend on the general properties of the target downstream functions. This dependence explains intriguing features of visual cells that are sensitive to binocular disparity and of neurons tuned to echo delay in bats. The numerical results suggest that optimal sensory tuning curves are shaped not only by stimulus statistics and signal-to-noise properties, but also according to their impact on downstream neural circuits and, ultimately, on behavior.Comment: 24 pages, 9 figures (main text + supporting information

Encoding and processing of sensory information in neuronal spike trains

Recently, a statistical signal-processing technique has allowed the information carried by single spike trains of sensory neurons on time-varying stimuli to be characterized quantitatively in a variety of preparations. In weakly electric fish, its application to first-order sensory neurons encoding electric field amplitude (P-receptor afferents) showed that they convey accurate information on temporal modulations in a behaviorally relevant frequency range (<80 Hz). At the next stage of the electrosensory pathway (the electrosensory lateral line lobe, ELL), the information sampled by first-order neurons is used to extract upstrokes and downstrokes in the amplitude modulation waveform. By using signal-detection techniques, we determined that these temporal features are explicitly represented by short spike bursts of second-order neurons (ELL pyramidal cells). Our results suggest that the biophysical mechanism underlying this computation is of dendritic origin. We also investigated the accuracy with which upstrokes and downstrokes are encoded across two of the three somatotopic body maps of the ELL (centromedial and lateral). Pyramidal cells of the centromedial map, in particular I-cells, encode up- and downstrokes more reliably than those of the lateral map. This result correlates well with the significance of these temporal features for a particular behavior (the jamming avoidance response) as assessed by lesion experiments of the centromedial map

Neuronal Synchronization Can Control the Energy Efficiency of Inter-Spike Interval Coding

The role of synchronous firing in sensory coding and cognition remains controversial. While studies, focusing on its mechanistic consequences in attentional tasks, suggest that synchronization dynamically boosts sensory processing, others failed to find significant synchronization levels in such tasks. We attempt to understand both lines of evidence within a coherent theoretical framework. We conceptualize synchronization as an independent control parameter to study how the postsynaptic neuron transmits the average firing activity of a presynaptic population, in the presence of synchronization. We apply the Berger-Levy theory of energy efficient information transmission to interpret simulations of a Hodgkin-Huxley-type postsynaptic neuron model, where we varied the firing rate and synchronization level in the presynaptic population independently. We find that for a fixed presynaptic firing rate the simulated postsynaptic interspike interval distribution depends on the synchronization level and is well-described by a generalized extreme value distribution. For synchronization levels of 15% to 50%, we find that the optimal distribution of presynaptic firing rate, maximizing the mutual information per unit cost, is maximized at ~30% synchronization level. These results suggest that the statistics and energy efficiency of neuronal communication channels, through which the input rate is communicated, can be dynamically adapted by the synchronization level.Comment: 47 pages, 14 figures, 2 Table

On palimpsests in neural memory: an information theory viewpoint

The finite capacity of neural memory and the reconsolidation phenomenon suggest it is important to be able to update stored information as in a palimpsest, where new information overwrites old information. Moreover, changing information in memory is metabolically costly. In this paper, we suggest that information-theoretic approaches may inform the fundamental limits in constructing such a memory system. In particular, we define malleable coding, that considers not only representation length but also ease of representation update, thereby encouraging some form of recycling to convert an old codeword into a new one. Malleability cost is the difficulty of synchronizing compressed versions, and malleable codes are of particular interest when representing information and modifying the representation are both expensive. We examine the tradeoff between compression efficiency and malleability cost, under a malleability metric defined with respect to a string edit distance. This introduces a metric topology to the compressed domain. We characterize the exact set of achievable rates and malleability as the solution of a subgraph isomorphism problem. This is all done within the optimization approach to biology framework.Accepted manuscrip