Cluster organization and response characteristics of the giant fiber pathway of the blowfly Calliphora erythrocephala

Abstract

Intersegmental descending neurons (DNs) link the insect brain to the thoracic ganglia. Iontophoresis of cobalt or fluorescent dyes reveals DNs as uniquely identifiable elements, the dendrites of which are situated within a characteristic region of the lateral deutocerebrum. Here we demonstrate that DNs occur as discrete groups of elements termed DN clusters (DNCs). A DNC is a characteristic combination of neurons that arises from a multiglomerular complex in which the main components of each glomerulus are a characteristic ensemble of sensory afferents. Other neurons involved in the complex are local interneurons, heterolateral interneurons that connect DNCs on both sides of the brain, and neurons originating in higher centers of the brain. We describe the structure, relationships, and projections of eight DNs that contribute to a descending neuron cluster located ventrally in the lateral deutocerebrum, an area interposed between the ventral antennal lobes and the laterally disposed optic lobes. We have named this cluster the GDNC because its most prominent member is the giant descending neuron (GDN), which plays a cardinal role in the midleg "jump" response and which is implicated in the initiation of flight. The GDN and its companion neurons receive primary mechanosensory afferents from the antennae, terminals of wide- and small-field retinotopic neurons originating in the lobula, and endings derived from sensory interneurons that originate in leg neuropil of the thoracic ganglia. We demonstrate that DNs of this cluster share morphological and functional properties. They have similar axon trajectories into the thoracic ganglia, where they invade functionally related neuropils. Neurons of the GDNC respond to identical stimulus paradigms and share similar electrophysiological characteristics. Neither the GDN nor other members of its cluster show spontaneous activity. These neurons are reluctant to respond to unimodal stimuli, but respond to specific combinations of visual and mechanosensory stimulation. These results suggest that in flies groups of morphologically similar DNs responding to context-specific environmental cues may cooperate in motor control.

Constitutive Activation of Ca2+/Calmodulin-Dependent Protein Kinase II during Development Impairs Central Cholinergic Transmission in a Circuit Underlying Escape Behavior inDrosophila

“…4 H). It has been suggested that this type of escape behavior can be induced in white-eyed mutants only Bacon and Strausfeld, 1986;Milde and Strausfeld, 1990;Fayyazuddin et al, 2006). In contrast, our experiments with transgenic animals expressing CaMKII in GFS or in cholinergic neurons show that it is not the eye color (red in our case), but probably the genetic background (w 1118 ) that is the decisive factor in eliciting this escape behavior.…”

On the coordination of motor output during visual flight control of flies

“…In contrast to locusts (for review, see Rowell 1988), however, not much is known about their physiology in flies, despite an extensive anatomical description (e.g. Strausfeld 1989;Milde and Strausfeld 1990;Strausfeld and Gronenberg 1990;Gronenberg and Strausfeld 1990).…”

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

“…In contrast, not all of them showed obvious responses to visual stimuli, including both light-off and dark-field expansion. A study of the blowfly Calliphora erythrocephala found that the GDN would spike when simultaneously given a mechanical stimulus to the antenna and a light-off stimulus to the eye (Milde and Strausfeld, 1990). Fig.…”

“…Descending neurons (DNs) mediating this alternative escape pathway have not yet been identified. Possible candidates are other members of the GDN cluster that comprise a system of at least eight parallel channels, which with the GDN likely share at least the same lobula-derived inputs (Strausfeld and Bacon, 1983;Milde and Strausfeld, 1990). More recent studies on the Drosophila GDN have shown that looming visual stimuli elicit subthreshold responses (Mu et al, 2012a), as do acoustic stimuli detected by the antenna's Johnston's organ (Tootoonian et al, 2012) or direct mechanical stimulation of the antenna (Lehnert et al, 2013).…”