Preserving Information in Neural Transmission

Beckman Vision Center, University of California, San Francisco, California 94143, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 05/2009; 29(19):6207-16. DOI: 10.1523/JNEUROSCI.3701-08.2009
Source: PubMed


Along most neural pathways, the spike trains transmitted from one neuron to the next are altered. In the process, neurons can either achieve a more efficient stimulus representation, or extract some biologically important stimulus parameter, or succeed at both. We recorded the inputs from single retinal ganglion cells and the outputs from connected lateral geniculate neurons in the macaque to examine how visual signals are relayed from retina to cortex. We found that geniculate neurons re-encoded multiple temporal stimulus features to yield output spikes that carried more information about stimuli than was available in each input spike. The coding transformation of some relay neurons occurred with no decrement in information rate, despite output spike rates that averaged half the input spike rates. This preservation of transmitted information was achieved by the short-term summation of inputs that geniculate neurons require to spike. A reduced model of the retinal and geniculate visual responses, based on two stimulus features and their associated nonlinearities, could account for >85% of the total information available in the spike trains and the preserved information transmission. These results apply to neurons operating on a single time-varying input, suggesting that synaptic temporal integration can alter the temporal receptive field properties to create a more efficient representation of visual signals in the thalamus than the retina.

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    • "In order to evaluate the information about the stimulus (PS) carried by individual spikes following a PS within T PS , we used the above calculated time varying firing rates r(t) and computed the entropy estimates (H) as follows (Strong et al., 1998; Brenner et. al., 2000; Sincich et al., 2009): "
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    ABSTRACT: In vivo, neurons establish functional connections and preserve information along their synaptic pathways from one information processing stage to the next in a very efficient manner. Paired spiking (PS) enhancement plays a key role by acting as a temporal filter that deletes less informative spikes. We analyzed the spontaneous neural activity evolution in a hippocampal and a cortical network over several weeks exploring whether the same PS coding mechanism appears in neuronal cultures as well. We show that self-organized neural in vitro networks not only develop characteristic bursting activity, but feature robust in vivo-like PS activity. PS activity formed spatiotemporal patterns that started at early days in vitro (DIVs) and lasted until the end of the recording sessions. Initially random-like and sparse PS patterns became robust after three weeks in vitro (WIVs). They were characterized by a high number of occurrences and short inter-paired spike intervals (IPSIs). Spatially, the degree of complexity increased by recruiting new neighboring sites in PS as a culture matured. Moreover, PS activity participated in establishing functional connectivity between different sites within the developing network. Employing transfer entropy (TE) as an information transfer measure, we show that PS activity is robustly involved in establishing effective connectivities. Spiking activity at both individual sites and network level robustly followed each PS within a short time interval. PS may thus be considered a spiking predictor. These findings suggest that PS activity is preserved in spontaneously active in vitro networks as part of a robust coding mechanism as encountered in vivo. We suggest that, presumably in lack of any external sensory stimuli, PS may act as an internal surrogate stimulus to drive neural activity at different developmental stages.
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    • "Many of these cells show encoding limits lower than 10 ms. Information rates measured in central neurons of different animals ranging from insects up to monkeys are much smaller than the ones typically found for sensory receptors (see for overview: Borst and Theunissen, 1999; fly H1 and monkey MT, (Strong et al., 1998); retinal ganglion cells (Koch et al., 2004; Passaglia and Troy, 2004); LGN neurons, (Sincich et al., 2009); V1 simple cells, (Reich et al., 2001). From these published data it seems reasonable to assume that peripheral receptors in general are optimized to convey maximal sensory information at fast rates. "
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    ABSTRACT: Sensory receptors determine the type and the quantity of information available for perception. Here, we quantified and characterized the information transferred by primary afferents in the rat whisker system using neural system identification. Quantification of ‘how much’ information is conveyed by primary afferents, using the direct method, a classical information theoretic tool, revealed that primary afferents transfer huge amounts of information (up to 529 bits/s). Information theoretic analysis of instantaneous spike-triggered kinematic stimulus features was used to gain functional insight on ‘what’ is coded by primary afferents. Amongst the kinematic variables tested - position, velocity, and acceleration - primary afferent spikes encoded velocity best. The other two variables contribute to information transfer, but only if combined with velocity. We further revealed three additional characteristics that play a role in information transfer by primary afferents. Firstly, primary afferent spikes show preference for well separated multiple stimuli (i.e. well separated sets of combinations of the three instantaneous kinematic variables). Secondly, spikes are sensitive to short strips of the stimulus trajectory (up to 10 ms pre-spike time), and thirdly, they show spike patterns (precise doublet and triplet spiking). In order to deal with these complexities, we used a flexible probabilistic neuron model fitting mixtures of Gaussians to the spike triggered stimulus distributions, which quantitatively captured the contribution of the mentioned features and allowed us to achieve a full functional analysis of the total information rate indicated by the direct method. We found that instantaneous position, velocity, and acceleration explained about 50% of the total information rate. Adding a 10 ms pre-spike interval of stimulus trajectory achieved 80-90%. The final 10-20% were found to be due to non-linear coding by spike bursts.
    Frontiers in Neural Circuits 12/2013; DOI:10.3389/fncir.2013.00190 · 3.60 Impact Factor
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    • "We found that the amount of information per spike decreased as the ISI increased. This finding, together with the previously presented results, suggests that ISI-based filtering of retinal spike trains is part of the mechanism that helps in preserving information about the important features of visual stimuli as it travels from retina to cortex, increasing the information efficiency to improve signaling the optimal stimulus features as has been suggested also by recent studies in macaque and cat [22] [23] [29] "
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    ABSTRACT: The information regarding visual stimulus is encoded in spike trains at the output of retina by retinal ganglion cells (RGCs). Among these, the directional selective cells (DSRGC) are signaling the direction of stimulus motion. DSRGCs' spike trains show accentuated periods of short interspike intervals (ISIs) framed by periods of isolated spikes. Here we use two types of visual stimulus, white noise and drifting bars, and show that short ISI spikes of DSRGCs spike trains are more often correlated to their preferred stimulus feature (that is, the direction of stimulus motion) and carry more information than longer ISI spikes. Firstly, our results show that correlation between stimulus and recorded neuronal response is best at short ISI spiking activity and decrease as ISI becomes larger. We then used grating bars stimulus and found that as ISI becomes shorter the directional selectivity is better and information rates are higher. Interestingly, for the less encountered type of DSRGC, known as ON-DSRGC, short ISI distribution and information rates revealed consistent differences when compared with the other directional selective cell type, the ON-OFF DSRGC. However, these findings suggest that ISI-based temporal filtering integrates a mechanism for visual information processing at the output of retina toward higher stages within early visual system.
    Computational Intelligence and Neuroscience 08/2012; 2012:918030. DOI:10.1155/2012/918030 · 0.60 Impact Factor
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