No 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.

In calliphorid Diptera, motor neurons mediating visually evoked head movements can be excited or inhibited by visual stimuli, depending on the directionality of the stimulus and whether it is in the ipsi- or contralateral visual field. The level at which inhibition occurs is of special interest because binocular activation of homolateral tangential neurons in the lobula plate demonstrates that excitatory interaction must occur between the left and right optic lobes. Recordings and dye fillings demonstrate a variety of motion-sensitive heterolateral pathways between the lobula plates, or between them and contralateral deutocerebral neuropil, which provides descending pathways to neck motor centers. The profiles of heterolateral tangential cells correspond to neurons stained by an antibody against gamma-aminobutyric acid (GABA). Other GABA-immunoreactive interneurons linking each side of the brain correspond to uniquely identified motion-sensitive neurons linking the deutocerebral. Additional inhibitory pathways include heterolateral GABAergic descending and ascending neurons, as well as heterolateral GABAergic neurons in the thoracic ganglia. The functional significance of heterolateral GABAergic pathways was tested surgically by making selective microlesions and monitoring the oculomotor output. The results demonstrate an important new attribute of the insect visual system. Although lesions can initially abolish an excitatory or inhibitory response, this response is reestablished through alternative pathways that provide inhibitory and excitatory information to the same motor neurons.

No 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.