Spike-like potentials in the axons of nonspiking photoreceptors

Weckström, Matti; Järvilehto, Matti; Heimonen, Kyösti

doi:10.1152/jn.1993.69.1.293

Cited by 16 publications

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“…At stimulus intensities of Ͻ10 photons/s, the bumps were large (up to 5-10 mV). In contrast to the ϳ100-fold variation in sensitivity of graded light responses (Heimonen et al 2006;Weckström et al 1993), the differences in the absolute sensitivity were ϳ10 times less. With the same dim background, the average bump frequency of different cells varied between two and 20 bumps/s (9 Ϯ 4 bumps/s; mean Ϯ SD; n ϭ 18).…”

Section: Resultsmentioning

confidence: 82%

“…The DA voltage responses were recorded first to show the variability as described before (Heimonen et al 2006) and secondly, to further study the LA as it is reflected in response shapes with long light pulses of up to 10 s. When dark adapted, the impulse responses of different types of photoreceptors were often similar. However, the cells could be distinguished by their ϳ100-fold sensitivity differences, as determined by their individual voltage vs. log of intensity (V-logI) curves (Heimonen et al 2006;Weckström et al 1993). With longer light pulses, differences in adaptation emerged (Figs.…”

Section: Resultsmentioning

confidence: 99%

“…Under a stereomicroscope, the retina of the cockroach is seen below the cornea as a black, highly pigmented area, and the location of recording electrode in the preparation could be identified on these grounds. This location is also characterized by graded-depolarizing responses, which lack the superimposed spikes typical for cockroach photoreceptor axon recordings (Heimonen et al 2006;Weckström et al 1993). No attempts were made to distinguish between the responses of the shortand long-type photoreceptors, which terminate in the first and second neuropile, respectively (Ribi 1977).…”

Section: Animals and Preparationmentioning

confidence: 99%

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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: Resultsmentioning

confidence: 82%

Section: Resultsmentioning

confidence: 99%

Section: Animals and Preparationmentioning

confidence: 99%

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Signal coding in cockroach photoreceptors is tuned to dim environments

Heimonen

Immonen

Frolov

et al. 2012

Journal of Neurophysiology

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“…Size and extent of the rhabdom vary, suggesting variation in photon capture efficiency, leading to variability in photoreceptor sensitivity, which is indeed found experimentally ( Fig. 2) (Butler and Horridge, 1973b;Weckström et al, 1993). In the more or less diffraction-limited compound eye, the ratio of axial distance between the lens and the rhabdom to the width of the rhabdom tip determines angular sensitivity (Snyder, 1977;Stavenga, 2003).…”

Section: How Is Variability Achieved?mentioning

confidence: 71%

“…2). Differences in sensitivity in dark-adapted state could vary even over two orders of magnitude (Butler and Horridge, 1973b;Weckström et al, 1993). The adaptational diversity of photoreceptors was even clearer in responses to saturating 10 s light pulses (Fig.…”

Section: Variability Of Sensitivity and Adaptation Speedmentioning

confidence: 99%

Large Functional Variability in Cockroach Photoreceptors: Optimization to Low Light Levels

Heimonen

Salmela²,

Kontiokari³

et al. 2006

J. Neurosci.

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The compound eyes of insects contain photoreceptors in small eyelets, ommatidia. The photoreceptors generally vary very little from ommatidium to ommatidium. However, in the large compound eyes of the cockroach (Periplaneta americana), previous studies have shown large differences in the optical structure between the ommatidia. The anatomy suggests pooling of 6 -20 photoreceptor signals into one second-order cell in the first synapse. Here, we show and characterize an unexpectedly large and seemingly random functional variability in the cockroach photoreceptors in terms of sensitivity, adaptation speed, angular sensitivity, and signal-to-noise ratio. We also investigate the implications of action potentials, triggered by the light-induced membrane depolarization in the photoreceptor axons. The combination of the functional features reported here is unique among the compound eyes. Recordings from the proximal parts of the thin and long photoreceptor axons or small and distant second-order neurons are not practical with the present methods. To alleviate this lack of data, we used computer simulations mimicking the functional variability, spike coding, and pooling of 12 photoreceptor signals, on the basis of our recordings from the photoreceptor somata and distal axons. The predicted responses of a simulated second-order cell follow surprisingly reliably the simulated light stimuli when compared with a simulation of functionally identical photoreceptors. We hypothesize that cockroach photoreceptors use action potential coding and a kind of population coding scheme for making sense of the inherently unreliable light signals at low luminance and for optimization of vision in its mainly dim living conditions.

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Voltage-activated outward currents in adult and nymphal locust photoreceptors

Weckström

1994

J Comp Physiol A

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The membrane properties of dark-adapted green sensitive photoreceptors of adult and nymphal desert locust (Schistocerca gregaria) were investigated in situ with single electrode (discontinuous) current and voltage clamp techniques. The photoreceptors had a resting potential of about -70 mV. The membrane rectified strongly in response to depolarizing current pulses at and above the resting potential. Two outward currents could be distinguished on the basis of different kinetics. The first, a transient current, was inactivating between -40 mV and -100 mV, and activated above -90 mV. The second, a sustained current had a similar activation range. The inactivating current could be blocked by application of 50 mM TEA into the retinal extracellular space. Both currents were expressed in nymphal photoreceptors already in the 1st instar larva and have similar properties as in the adults, although the behaviour of adults and nymphs is different. The conductances underlying these currents could be shown to modify the frequency response of the photoreceptor membrane.

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Spike-like potentials in the axons of nonspiking photoreceptors

Cited by 16 publications

References 0 publications

Signal coding in cockroach photoreceptors is tuned to dim environments

Signal coding in cockroach photoreceptors is tuned to dim environments

Large Functional Variability in Cockroach Photoreceptors: Optimization to Low Light Levels

Voltage-activated outward currents in adult and nymphal locust photoreceptors

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