A Novel Estimator for the Rate of Information Transfer by Continuous Signals

Takalo, Jouni; Ignatova, Irina I.; Weckström, Matti; Vähäsöyrinki, Mikko

doi:10.1371/journal.pone.0018792

Cited by 6 publications

(8 citation statements)

References 19 publications

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“…For a purely linear measure, such as the one obtained from the SNR(f) by using the Shannon (1948) formula for information capacity, the estimated information transfer rate is limited below ϳ45 bits/s. The high rates (Ͼ100 bits/s) were obtained only with NIS stimulation and a novel information rate estimator (Juusola and de Polavieja 2003;Takalo et al 2011), which does not assume linearity of the system or Gaussian distribution of the signals. Hence, the signaling mechanisms in cockroach photoreceptors appear to be highly adapted to naturalistic light changes, which contain long, darker periods that are likely to foster recovery of microvilli from the refractory state.…”

Section: Discussionmentioning

confidence: 99%

Signal coding in cockroach photoreceptors is tuned to dim environments

Heimonen

Immonen

Frolov

et al. 2012

Journal of Neurophysiology

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Heimonen K, Immonen E-V, Frolov RV, Salmela I, Juusola M, Vähäsöyrinki M, Weckström M. Signal coding in cockroach photoreceptors is tuned to dim environments. J Neurophysiol 108: 2641-2652, 2012. First published August 29, 2012 doi:10.1152/jn.00588.2012.-In dim light, scarcity of photons typically leads to poor vision. Nonetheless, many animals show visually guided behavior with dim environments. We investigated the signaling properties of photoreceptors of the dark active cockroach (Periplaneta americana) using intracellular and whole-cell patch-clamp recordings to determine whether they show selective functional adaptations to dark. Expectedly, darkadapted photoreceptors generated large and slow responses to single photons. However, when light adapted, responses of both phototransduction and the nontransductive membrane to white noise (WN)-modulated stimuli remained slow with corner frequencies ϳ20 Hz. This promotes temporal integration of light inputs and maintains high sensitivity of vision. Adaptive changes in dynamics were limited to dim conditions. Characteristically, both step and frequency responses stayed effectively unchanged for intensities Ͼ1,000 photons/s/photoreceptor. A signal-to-noise ratio (SNR) of the light responses was transiently higher at frequencies Ͻ5 Hz for ϳ5 s after light onset but deteriorated to a lower value upon longer stimulation. Naturalistic light stimuli, as opposed to WN, evoked markedly larger responses with higher SNRs at low frequencies. This allowed realistic estimates of information transfer rates, which saturated at ϳ100 bits/s at low-light intensities. We found, therefore, selective adaptations beneficial for vision in dim environments in cockroach photoreceptors: large amplitude of single-photon responses, constant high level of temporal integration of light inputs, saturation of response properties at low intensities, and only transiently efficient encoding of light contrasts. The results also suggest that the sources of the large functional variability among different photoreceptors reside mostly in phototransduction processes and not in the properties of the nontransductive membrane.vision; systems analysis; adaptation; temporal resolution; photons SENSORY SYSTEMS PROVIDE ANIMALS with necessary information for survival and reproduction. Like all senses of different species, visual systems are thought to have selectively adapted for functioning under their prevailing environmental conditions during their evolution and development

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Section: Discussionmentioning

confidence: 99%

Signal coding in cockroach photoreceptors is tuned to dim environments

Heimonen

Immonen

Frolov

et al. 2012

Journal of Neurophysiology

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“…Young (2-6 days posteclosion) female blowflies (Calliphora vicina) were used in all experiments. Preparation and intracellular recordings were performed from broadband photoreceptors as described previously (Juusola et al 1994;Takalo et al 2011). In brief, alumosilicate microelectrodes (Harvard Apparatus) were manufactured using a laser puller (P-2000; Sutter Instruments) and filled with 2 M potassium acetate solution; microelectrodes had resistances in the range of 100 -130 M⍀.…”

Section: Experimental Designmentioning

confidence: 99%

“…Mutual information (MI) can be defined as MI ϭ H(X) ϩ H(Y) -H(X, Y), where H(X) and H(Y) are the entropies of the input and output, respectively, and H(X,Y) is the joint entropy of X and Y. Mutual information rate R was calculated from the equation MI ϭ R•d ϩ c, where d is the dimension of the random process and c is a constant depending on the initial condition (Takalo et al 2011). R was estimated in nats/sample units as the linear slope of MI function of a dimension d and then this measure was divided by the sample interval and by log2 to yield bits/s units.…”

Section: Experimental Designmentioning

confidence: 99%

Effects of phase correlations in naturalistic stimuli on quantitative information coding by fly photoreceptors

Ignatova

French

Frolov

2018

Journal of Neurophysiology

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Natural visual scenes are rarely random. Instead, intensity and wavelength change slowly in time and space over many regions of the scene, so that neighboring temporal and spatial visual inputs are more correlated and contain less information than truly random signals. It has been suggested that sensory optimization to match these higher order correlations (HOC) occurs at the earliest visual stages, and that photoreceptors can process temporal natural signals more efficiently than random signals. We tested this early-stage hypothesis by comparing the information content of Calliphora vicina photoreceptor responses to naturalistic inputs before and after removing HOC by randomizing phase. Forty different, 60-s long, naturalistic sequences (NS) were used, together with randomized-phase versions of the same sequences to give pink noise (PN) so that each input pair had identical means, variances, mean contrasts, and power spectra. We measured the information content of inputs and membrane potential responses by three different methods: coherence, mutual information, and compression entropy. We also used entropy and phase statistics of each pair as measures of HOC. Responses to randomized signals generally had higher gain, signal-to-noise ratio, and information rates than responses to NS. Information rate increased with a strong, positive, linear correlation to phase randomization within sequence pairs. This was confirmed by varying the degree of phase randomization. Our data indicate that individual photoreceptors encode input information by Weber's law, with HOC within natural sequences reducing information transfer by decreasing the number of local contrast events that exceed the noise-imposed threshold. NEW & NOTEWORTHY Natural visual scenes feature statistical regularities, or higher order correlations (HOC), both in time and space, to encode surfaces, textures, and object boundaries. Visual systems rely on this information; however, it remains controversial whether individual photoreceptors can discriminate and enhance information encoded in HOC. Here we show that the more HOC the stimulus contains, the lower the information transfer rate of photoreceptors. We explain our findings by applying the Weber's paradigm of differential signal perception.

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“…In vivo intracellular single-electrode recordings were performed as described previously [29]. In brief, for intracellular recordings, backswimmers were maintained in reversed 12 -12 illumination conditions with a subjective 'night' period matching the actual day (regimen 2; see below for details).…”

Section: (B) In Vivo Intracellular Single-electrode Recordingsmentioning

confidence: 99%

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

et al. 2014

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The common backswimmer, Notonecta glauca, uses vision by day and night for functions such as underwater prey animal capture and flight in search of new habitats. Although previous studies have identified some of the physiological mechanisms facilitating such flexibility in the animal's vision, neither the biophysics of Notonecta photoreceptors nor possible cellular adaptations are known. Here, we studied Notonecta photoreceptors using patch-clamp and intracellular recording methods. Photoreceptor size (approximated by capacitance) was positively correlated with absolute sensitivity and acceptance angles. Information rate measurements indicated that large and more sensitive photoreceptors performed better than small ones. Our results suggest that backswimmers are adapted for vision in both dim and wellilluminated environments by having open-rhabdom eyes with large intrinsic variation in absolute sensitivity among photoreceptors, exceeding those found in purely diurnal or nocturnal species. Both electrophysiology and microscopic analysis of retinal structure suggest two retinal subsystems: the largest peripheral photoreceptors provide vision in dim light and the smaller peripheral and central photoreceptors function primarily in sunlight, with light-dependent pigment screening further contributing to adaptation in this system by dynamically recruiting photoreceptors with varying sensitivity into the operational pool.

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A Novel Estimator for the Rate of Information Transfer by Continuous Signals

Cited by 6 publications

References 19 publications

Signal coding in cockroach photoreceptors is tuned to dim environments

Signal coding in cockroach photoreceptors is tuned to dim environments

Effects of phase correlations in naturalistic stimuli on quantitative information coding by fly photoreceptors

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

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