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Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors.

Salmela I, Immonen EV, Frolov R, Krause S, Krause Y, Vähäsöyrinki M, Weckström M - BMC Neurosci (2012)

Bottom Line: Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA).However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Physics, University of Oulu, Oulu, Finland.

ABSTRACT

Background: The importance of voltage-dependent conductances in sensory information processing is well-established in insect photoreceptors. Here we present the characterization of electrical properties in photoreceptors of the cockroach (Periplaneta americana), a nocturnal insect with a visual system adapted for dim light.

Results: Whole-cell patch-clamped photoreceptors had high capacitances and input resistances, indicating large photosensitive rhabdomeres suitable for efficient photon capture and amplification of small photocurrents at low light levels. Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA). Activation of KDR occurred during physiological voltage responses induced by light stimulation, whereas KA was nearly fully inactivated already at the dark resting potential. In addition, hyperpolarization of photoreceptors activated a small-amplitude inward-rectifying (IR) current mediated at least partially by chloride. Computer simulations showed that KDR shapes light responses by opposing the light-induced depolarization and speeding up the membrane time constant, whereas KA and IR have a negligible role in the majority of cells. However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.

Conclusions: The relative expression of KA and KDR in cockroach photoreceptors was opposite to the previously hypothesized framework for dark-active insects, necessitating further comparative work on the conductances. In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

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General features of isolated photoreceptors. A) Isolated ommatidia of Periplaneta americana.  Single photoreceptors cluster with their fused rhabdom concentrically around the longitudinal axis of the ommatidium. The rhabdom can be recognized as a dark central structure. Lenses at the distal end (top) and axons at the proximal end (bottom) are ripped off during isolation. Note the pigmentation of the ommatidia. B) Whole-cell capacitances of green-sensitive photoreceptor cells (n = 45). C) Current responses to 1 ms dim light flash stimuli containing less than 1 photon on average showed both single photon absorptions (+) and failures (-). The variability of response latency and amplitude reflects the random properties of phototransduction. The holding potential in voltage clamp mode was -77 mV. D) Voltage responses (top) and corresponding light-induced-currents (middle) to a 10 s long naturalistic light intensity series (bottom) recorded in whole-cell patch clamp. Relative intensities were 1 (gray traces) and 10 (black trace). E) In whole-cell current clamp recordings, voltage responses (top) to current injections (bottom) exhibited both inward- and outward rectification, indicating the presence of voltage-dependent conductances. The small-amplitude depolarizations are single photon responses to ambient light.
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Figure 1: General features of isolated photoreceptors. A) Isolated ommatidia of Periplaneta americana. Single photoreceptors cluster with their fused rhabdom concentrically around the longitudinal axis of the ommatidium. The rhabdom can be recognized as a dark central structure. Lenses at the distal end (top) and axons at the proximal end (bottom) are ripped off during isolation. Note the pigmentation of the ommatidia. B) Whole-cell capacitances of green-sensitive photoreceptor cells (n = 45). C) Current responses to 1 ms dim light flash stimuli containing less than 1 photon on average showed both single photon absorptions (+) and failures (-). The variability of response latency and amplitude reflects the random properties of phototransduction. The holding potential in voltage clamp mode was -77 mV. D) Voltage responses (top) and corresponding light-induced-currents (middle) to a 10 s long naturalistic light intensity series (bottom) recorded in whole-cell patch clamp. Relative intensities were 1 (gray traces) and 10 (black trace). E) In whole-cell current clamp recordings, voltage responses (top) to current injections (bottom) exhibited both inward- and outward rectification, indicating the presence of voltage-dependent conductances. The small-amplitude depolarizations are single photon responses to ambient light.

Mentions: Isolated cockroach ommatidia were between 100 and 150 μm long and ca. 30 μm wide (Figure 1A) and normally did not contain the photoreceptor axons. In patch clamp experiments, the seal resistance was typically greater than 10 GΩ and the whole-cell input resistance (Rin) in darkness varied between 200 MΩ and 10 GΩ (Rin = 1.6 ± 2.4 GΩ, n = 32). The Rin values were larger than the previous estimates from in vivo intracellular recordings [26,27], possibly because of the absence of a membrane leak due to membrane piercing with a sharp glass microelectrode [29]. Whole-cell membrane capacitance was measured as a proxy for the membrane area and cell size, which are known to vary within single ommatidia [30]. The capacitances ranged from 100 to 800 pF (Figure 1B) and did not follow a normal distribution, which may reflect different photoreceptor size groups in the ommatidia [30]. We cannot rule out the possibility that some recordings with the largest capacitances could contain more than one cell. However, such occurrences have not been reported before with insect photoreceptors in patch clamp, although in intracellular recordings it is possible [31].


Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors.

Salmela I, Immonen EV, Frolov R, Krause S, Krause Y, Vähäsöyrinki M, Weckström M - BMC Neurosci (2012)

General features of isolated photoreceptors. A) Isolated ommatidia of Periplaneta americana.  Single photoreceptors cluster with their fused rhabdom concentrically around the longitudinal axis of the ommatidium. The rhabdom can be recognized as a dark central structure. Lenses at the distal end (top) and axons at the proximal end (bottom) are ripped off during isolation. Note the pigmentation of the ommatidia. B) Whole-cell capacitances of green-sensitive photoreceptor cells (n = 45). C) Current responses to 1 ms dim light flash stimuli containing less than 1 photon on average showed both single photon absorptions (+) and failures (-). The variability of response latency and amplitude reflects the random properties of phototransduction. The holding potential in voltage clamp mode was -77 mV. D) Voltage responses (top) and corresponding light-induced-currents (middle) to a 10 s long naturalistic light intensity series (bottom) recorded in whole-cell patch clamp. Relative intensities were 1 (gray traces) and 10 (black trace). E) In whole-cell current clamp recordings, voltage responses (top) to current injections (bottom) exhibited both inward- and outward rectification, indicating the presence of voltage-dependent conductances. The small-amplitude depolarizations are single photon responses to ambient light.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC3472236&req=5

Figure 1: General features of isolated photoreceptors. A) Isolated ommatidia of Periplaneta americana. Single photoreceptors cluster with their fused rhabdom concentrically around the longitudinal axis of the ommatidium. The rhabdom can be recognized as a dark central structure. Lenses at the distal end (top) and axons at the proximal end (bottom) are ripped off during isolation. Note the pigmentation of the ommatidia. B) Whole-cell capacitances of green-sensitive photoreceptor cells (n = 45). C) Current responses to 1 ms dim light flash stimuli containing less than 1 photon on average showed both single photon absorptions (+) and failures (-). The variability of response latency and amplitude reflects the random properties of phototransduction. The holding potential in voltage clamp mode was -77 mV. D) Voltage responses (top) and corresponding light-induced-currents (middle) to a 10 s long naturalistic light intensity series (bottom) recorded in whole-cell patch clamp. Relative intensities were 1 (gray traces) and 10 (black trace). E) In whole-cell current clamp recordings, voltage responses (top) to current injections (bottom) exhibited both inward- and outward rectification, indicating the presence of voltage-dependent conductances. The small-amplitude depolarizations are single photon responses to ambient light.
Mentions: Isolated cockroach ommatidia were between 100 and 150 μm long and ca. 30 μm wide (Figure 1A) and normally did not contain the photoreceptor axons. In patch clamp experiments, the seal resistance was typically greater than 10 GΩ and the whole-cell input resistance (Rin) in darkness varied between 200 MΩ and 10 GΩ (Rin = 1.6 ± 2.4 GΩ, n = 32). The Rin values were larger than the previous estimates from in vivo intracellular recordings [26,27], possibly because of the absence of a membrane leak due to membrane piercing with a sharp glass microelectrode [29]. Whole-cell membrane capacitance was measured as a proxy for the membrane area and cell size, which are known to vary within single ommatidia [30]. The capacitances ranged from 100 to 800 pF (Figure 1B) and did not follow a normal distribution, which may reflect different photoreceptor size groups in the ommatidia [30]. We cannot rule out the possibility that some recordings with the largest capacitances could contain more than one cell. However, such occurrences have not been reported before with insect photoreceptors in patch clamp, although in intracellular recordings it is possible [31].

Bottom Line: Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA).However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Physics, University of Oulu, Oulu, Finland.

ABSTRACT

Background: The importance of voltage-dependent conductances in sensory information processing is well-established in insect photoreceptors. Here we present the characterization of electrical properties in photoreceptors of the cockroach (Periplaneta americana), a nocturnal insect with a visual system adapted for dim light.

Results: Whole-cell patch-clamped photoreceptors had high capacitances and input resistances, indicating large photosensitive rhabdomeres suitable for efficient photon capture and amplification of small photocurrents at low light levels. Two voltage-dependent potassium conductances were found in the photoreceptors: a delayed rectifier type (KDR) and a fast transient inactivating type (KA). Activation of KDR occurred during physiological voltage responses induced by light stimulation, whereas KA was nearly fully inactivated already at the dark resting potential. In addition, hyperpolarization of photoreceptors activated a small-amplitude inward-rectifying (IR) current mediated at least partially by chloride. Computer simulations showed that KDR shapes light responses by opposing the light-induced depolarization and speeding up the membrane time constant, whereas KA and IR have a negligible role in the majority of cells. However, larger KA conductances were found in smaller and rapidly adapting photoreceptors, where KA could have a functional role.

Conclusions: The relative expression of KA and KDR in cockroach photoreceptors was opposite to the previously hypothesized framework for dark-active insects, necessitating further comparative work on the conductances. In general, the varying deployment of stereotypical K+ conductances in insect photoreceptors highlights their functional flexibility in neural coding.

Show MeSH
Related in: MedlinePlus