Distribution of GABA-like immunoreactive neurons in the optic lobes of Periplaneta americana

Füller, Horst; Eckert, Manfred; Blechschmidt, K.

doi:10.1007/bf00229085

Cited by 22 publications

(25 citation statements)

References 21 publications

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“…The situation in the cockroach is different. Previous studies indicate a large degree of variation in structure of the compound eye and photoreceptors (Butler, 1971(Butler, , 1973aRibi, 1977;Ernst and Füller, 1987;Füller et al, 1989;Ferrell and Reitcheck, 1993). Lenses and rhabdoms have variable sizes and shapes.…”

Section: Discussionmentioning

confidence: 98%

“…5). In addition to large structural variability (Butler, 1971(Butler, , 1973aRibi, 1977;Ernst and Füller, 1987;Füller et al, 1989), all of these functional properties showed large inter-photoreceptor variation of up to two orders of magnitude. The variability in cockroach photoreceptors was randomly distributed all over the eye (the most ventral part and the margin of the eye were not studied).…”

Section: Variability Of Light Responsesmentioning

confidence: 99%

“…The anatomical investigations of the trajectories of photoreceptor axons suggest pooling of several (maybe 6 -20) photoreceptor responses on every second-order cell in the first optic neuropil, the lamina (Ribi, 1977;Ernst and Füller, 1987;Füller et al, 1989). The anatomy of the lamina is not known in detail.…”

Section: Hypothesis and Simulationmentioning

confidence: 99%

“…Anatomical data suggest a large amount of pooling in the first visual synapse (Ribi, 1977;Ernst and Füller, 1987;Füller et al, 1989). The functional variability of cockroach photoreceptors, especially within the same adaptational state, has not been properly characterized before, and this characterization forms a major part of this paper.…”

Section: Introductionmentioning

confidence: 96%

“…In contrast, a fair amount of structural and functional variation has been found in cockroach photoreceptors. The morphology, optics, and photoreceptors of cockroach ommatidia are irregular (Butler, 1971(Butler, , 1973aFüller et al, 1989), leading to degradation of the sampled image (French et al, 1977). The anatomy and length of photoreceptor axons varies a lot (Ribi, 1977;Ernst and Füller, 1987), although they are all thin and long (300 -1500 m) in comparison to most insects.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 98%

Section: Variability Of Light Responsesmentioning

confidence: 99%

Section: Hypothesis and Simulationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Heimonen

Salmela²,

Kontiokari³

et al. 2006

J. Neurosci.

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Distribution of GABA-like immunoreactive neurons in insects suggests lineage homology

Witten

Truman

1998

J. Comp. Neurol.

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Gamma-aminobutyric acid (GABA) is an important inhibitory neurotransmitter in vertebrates and invertebrates (Sattelle [1990] Adv. Insect Physiol. 22:1-113). The GABA phenotype is lineally determined in postembryonic neurons in the tobacco hawkmoth, Manduca sexta (Witten and Truman, [1991] J. Neurosci. 11:1980-1989) and is restricted to six identifiable postembryonic lineages in the moth's thoracic hemiganglia. We used a comparative approach to determine whether this distinct clustering of GABAergic neurons is conserved in Insecta. In the nine orders of insects surveyed (Thysanura, Odonata, Orthoptera, Isoptera, Hemiptera, Coleoptera, Diptera, Lepidoptera, and Hymenoptera), GABA-like immunoreactive neurons within a thoracic hemiganglion were clustered into six distinct groups that occupied positions similar to the six postembryonic lineages in Manduca. On the basis of cell body position and axon trajectories, we suggest that these are indeed homologous lineage groups and that the lineal origins of the GABAergic cells have been very conservative through insect evolution. The distinctive clustering of GABA-positive cells is shared with crustaceans (Mulloney and Hall [1990] J. Comp. Neurol. 291:383-394; Homberg et al. [1993] Cell Tissue Res. 271:279-288) but is not found in the centipede Lithobius forficulatus. There is a two- to threefold increase in numbers of thoracic neurons between the flightless Thysanura and the most advanced orders of insects. Using the GABA clusters as indicators of specific lineages, we find that only selected lineages have significantly contributed to this increase in neuronal numbers.

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Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa

Sinakevitch

Douglass

Scholtz

et al. 2003

J of Comparative Neurology

119

112

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The shared organization of three optic lobe neuropils-the lamina, medulla, and lobula-linked by chiasmata has been used to support arguments that insects and malacostracans are sister groups. However, in certain insects, the lobula is accompanied by a tectum-like fourth neuropil, the lobula plate, characterized by wide-field tangential neurons and linked to the medulla by uncrossed axons. The identification of a lobula plate in an isopod crustacean raises the question of whether the lobula plate of insects and isopods evolved convergently or are derived from a common ancestor. This question is here investigated by comparisons of insect and crustacean optic lobes. The basal branchiopod crustacean Triops has only two visual neuropils and no optic chiasma. This finding contrasts with the phyllocarid Nebalia pugettensis, a basal malacostracan whose lamina is linked by a chiasma to a medulla that is linked by a second chiasma to a retinotopic outswelling of the lateral protocerebrum, called the protolobula. In Nebalia, uncrossed axons from the medulla supply a minute fourth optic neuropil. Eumalacostracan crustaceans also possess two deep neuropils, one receiving crossed axons, the other uncrossed axons. However, in primitive insects, there is no separate fourth optic neuropil. Malacostracans and insects also differ in that the insect medulla comprises two nested neuropils separated by a layer of axons, called the Cuccati bundle. Comparisons suggest that neuroarchitectures of the lamina and medulla distal to the Cuccati bundle are equivalent to the eumalacostracan lamina and entire medulla. The occurrence of a second optic chiasma and protolobula are suggested to be synapomorphic for a malacostracan/insect clade.

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Distribution of GABA-like immunoreactive neurons in the optic lobes of Periplaneta americana

Cited by 22 publications

References 21 publications

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

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

Distribution of GABA-like immunoreactive neurons in insects suggests lineage homology

Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa

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