Oculomotor control in calliphorid flies: Organization of descending neurons to neck motor neurons responding to visual stimuli

Abstract

In insects, head movements are mediated by neck muscles supplied by nerves originating in the brain and prothoracic ganglion. Extracellular recordings of the nerves demonstrate units that respond to visual stimulation of the compound eyes and to mechanosensory stimulation of the halteres. The number of neck muscles required for optokinetic eye movements in flies is not known, although in other taxa, eye movements can involve as few as three pairs of muscles. This study investigates which neck motor neurons are likely to be involved in head movements by examining the relationships between neck muscle motor neurons and the terminals visiting them from approximately 50 pairs of descending neurons. Many of these descending neurons have dendrites in neuropils that are associated with modalities other than vision, and recording show that visual stimuli activate only a few neck motor neurons, such as the sclerite depressor neurons, which respond to local or wide-field, directionally specific motion, as do a subset of descending neurons coupled to them. The results suggest that, like in the vertebrate eye or the retinas of jumping spiders, optokinetic head movements of flies require only a few muscles. In addition to the importance of visual inputs, a major supply to neck muscle centers by nonvisual descending neurons suggests a role for tactile, gustatory, and olfactory signals in controlling head position.

Nonlinear Integration of Binocular Optic Flow by DNOVS2, A Descending Neuron of the Fly

“…These frontal nerve neck neurons in turn innervate the large sclerite depressor muscle involved in head-roll movements Gilbert et al, 1995). Previous studies showed that motor neurons of the frontal nerve are motion sensitive Gronenberg et al, 1995;Huston and Krapp, 2003;Krapp and Huston, 2005). Although the number of neck muscle and motor neurons is manageable Strausfeld et al, 1987), the neural circuit as well as the computations underlying these optomotor responses is complex and far from being understood.…”

“…Like DNOVS2, DNOVS1 projects from the axon terminals of VS cells into the thoracic ganglion and from there onto motor neurons (Strausfeld and Bassemir, 1985;Gronenberg et al, 1995). Both cells receive visual motion input via the VS cells and from the photoreceptors of the ocelli via L-neurons (Strausfeld and Bassemir, 1985;.…”

“…Gronenberg et al (1995) showed that the neuron responds to light ON, to antennal air currents, and to visual motion and is biocytin coupled to neck motor neurons, which mediate head rotation Gilbert et al, 1995). Here we demonstrate that DNOVS2 is specifically connected to LPTCs and tuned in a supralinear way to rotation around the longitudinal body axis.…”

Motor output reflects the linear superposition of visual and olfactory inputs inDrosophila

“…To our knowledge, this is the only reported example of an identified descending neuron that is selective for visual and olfactory cues. However, cells that integrate visual and mechanosensory information in other insects are not uncommon (Baader et al, 1992;Gronenberg et al, 1995;Olberg, 1981;Rowell and Reichert, 1986). Examining the physiological properties of as yet unidentified DNs in Drosophila will help define physiological mechanisms of sensorimotor superposition.…”

Integration of Lobula Plate Output Signals by DNOVS1, an Identified Premotor Descending Neuron

“…In this article, we present electrophysiological data on a specific descending neuron, the DNOVS1 (also called DNDC 1-1 by Gronenberg et al, 1995). Given the described connectivity to VS cells, we studied how the signals of a subset of VS cells and ocellar input are integrated on the dendrite of DNOVS1.…”