The relevance of neural architecture to visual performance: Phylogenetic conservation and variation in dipteran visual systems

Abstract

In cyclorrhaphan flies, giant tangential neurons in the lobula plate are supplied by isomorphic arrays of evolutionarily conserved achromatic elementary motion detecting circuits originating in the retina. The arrangements among giant tangential neurons is characteristic of a taxon and can differ between taxa having different visual performances. Observations of 12 brachyceran and 4 nematoceran species have identified different behaviors associated with visually stabilized flight. Neuroanatomical comparisons between closely related species having different behaviors and phylogenetically distant species that have similar behaviors suggest that such differences relate to differences of giant tangential cell architecture in the lobula plate. These functionally related differences contrast to anatomical features that reflect phylogenetic affinities. For example, the lobula plates of robber flies, typified by ballistic flight behavior, all differ from other taxa in lacking cyclorrhaphan-type vertical motion-sensitive neurons; instead, they possess an extra complement of horizontal cells in their place. The results suggest that, although circuits that compute elementary motion are conserved across the Diptera, selective pressure has resulted in modifications of their target neurons, thus contributing to the wide variety of visual behaviors observed within this group of insects.

A `bright zone' in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity

“…Furthermore, modeling efforts have shown that biologically inspired models based on such matched filters can accurately estimate the components of optical flow due to self translation and rotation in a rapid, feed-forward manner (Dahmen et al, 2001;Franz et al, 2004;Franz and Krapp, 2000). In other flies, the LPD organization is largely unknown, although the subject is of inherent interest because anatomical (Buschbeck and Strausfeld, 1997) and physiological (O'Carroll et al, 1996;O'Carroll et al, 1997) characteristics of LPTCs vary in a correlated manner with visual behavior. Yet smallfield motion-sensitive neurons of the medulla and pre-synaptic to LPTCs are highly conserved at the anatomical level (Buschbeck and Strausfeld, 1996), suggesting that the anatomy and physiology of LPTCs may have high 'evolutionary plasticity' that underlies behavioral differences between groups within the flies.…”

Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours

“…There are well-documented examples of species differences in sensory systems (Shaw & Meinertzhagen 1986;Shaw & Moore 1989;Boyan 1993;Mizunami 1995;Buschbeck & Strausfeld 1997). There is also much support for respecification of motor neurons (Sillar & Heitler 1985;Paul 1991;Katz & Tazaki 1992;Wright 2000;Chiang et al 2006), brain nuclei (Heiligenburg et al 1996) and entire brain regions (Karten 1991;Krubitzer 1995;Catania et al 1999;Catania 2000;Kaas 2004).…”

Generation and Evolution of Neural Cell Types and Circuits: Insights from the Drosophila Visual System

“…More subtle differences in the morphology of LMCs have been recorded between different species of Diptera (17, 20), but it is not clear whether such finer-scale differences in arborization patterns influence function. For instance, L2 and L5 exhibit different branching patterns in species in the Glossinidae, Asilidae, and Tabanidae (the horse and deer flies) (17).…”