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Early Visual Processing in the Compound Eye: Physiology and Pharmacology of the Retina-Lamina Projection in the Fly

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Neurobiology of Sensory Systems

Abstract

The defined physiology and anatomy of the retina and the first optic ganglion of the fly provide an excellent opportunity to study the neural mechanisms responsible for early visual processing. Intracellular recordings from an intact preparation have been used to analyse synaptic transfer from the photoreceptors to a major class of second order neurones, the large monopolar cells (LMCs). Coding is optimised to protect pictorial information from contamination by the noise generated at the photoreceptor synapses. Optimisation involves processes of amplification and antagonism that are matched to the statistical properties of images. Having derived a detailed description of coding, we are investigating the underlying physiological and pharmacological mechanisms. The synaptic transfer function has been determined by precise measurements of the responses of photoreceptors and LMCs to identical stimuli; noise analysis identifies a significant contribution of synaptic noise to the postsynaptic signal. Single-electrode current clamp analysis of the LMCs shows that their membranes are approximately Ohmic, so that voltage sensitive mechanisms play little role in signal-shaping. To a first approximation, LMC “on” responses can be described in terms of a single chloride conductance activated by the photoreceptor neurotransmitter, however, the depolarising transient generated at light “off” involves additional depolarizing mechanisms. Lateral inhibition is associated with a conductance decrease thus suggesting a presynaptic mechanism, and is under dynamic control, developing rapidly at the onset of light adaptation. It may vary in strength between different classes of LMC. Ionophoretic studies indicate that histamine mimics the photoreceptor neurotransmitter and the photoreceptor terminals show histamine-like immunoreactivity. This represents the first case of histaminergic neurotransmission in insects, and a pharmacological profile of the putative histamine receptors indicates that they are of a novel class. Immunocytochemical and ionophoretic studies also indicate the involvement of a number of classical neurotransmitters in other lamina interneurones.

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Author notes

  1. Daniel Osorio

    Present address: Centre for Visual Sciences, RSBS ANU Canberra, Australia

Authors and Affiliations

  1. Department of Zoology, Cambridge University, Downing St, Cambridge, UK

    Roger Hardie, Simon Laughlin & Daniel Osorio

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  1. Roger Hardie
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  2. Simon Laughlin
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Editors and Affiliations

  1. Tata Institute of Fundamental Research, Bombay, India

    R. Naresh Singh

  2. The University of Arizona, Tucson, Arizona, USA

    Nicholas J. Strausfeld

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Hardie, R., Laughlin, S., Osorio, D. (1989). Early Visual Processing in the Compound Eye: Physiology and Pharmacology of the Retina-Lamina Projection in the Fly. In: Singh, R.N., Strausfeld, N.J. (eds) Neurobiology of Sensory Systems. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-2519-0_3

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  • DOI: https://doi.org/10.1007/978-1-4899-2519-0_3

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