Central gating of fly optomotor response

Abstract

We study the integration of multisensory and central input at the level of an identified fly motoneuron, the ventral cervical nerve motoneuron (VCNM) cell, which controls head movements of the animal. We show that this neuron receives input from a central neuron signaling flight activity, from two identified wide-field motion-sensitive neurons, from the wind-sensitive Johnston organ on the antennae, and from the campaniform sensillae of the halteres. We find that visual motion alone leads to only subthreshold responses. Only when it is combined with flight activity or wind stimuli does the VCNM respond to visual motion by modulating its spike activity in a directionally selective way. This nonlinear enhancement of visual responsiveness in the VCNM by central activity is reflected at the behavioral level, when compensatory head movements are measured in response to visual motion. While head movements of flies have only a small amplitude when flies are at rest, the response amplitude is increased by a factor of 30-40 during flight.behavioral state | electrophysiology | motion vision | proprioceptor T he perceptual response to a sensory stimulus depends on the behavioral state of the animal. This is especially evident when responses between awake and sleeping or anesthetized animals are compared (1-5). In addition, attention can strongly modulate the perceptual response (6-11). Furthermore, recent studies have shown that the response properties of sensory neurons depend on the locomotor state of the animal (12-16). However, it is not clear at what level of the nervous system the integration of sensory input and internal state occurs and according to which rules. We address this question in an identified ventral cervical nerve motoneuron (VCNM) that is part of the neck motor system of the blowfly Calliphora vicina.Blowflies are well known for their aerobatic maneuvers. This flight behavior has important consequences for vision, because fast turns can lead to motion blur and thus impair vision of spatial details. These adverse effects on vision can, in principle, be partly compensated for by eye movements. However, in all insects, the eyes are fixed to the head capsule and only small eye movements are possible (17). Therefore, effective compensatory eye movements can only be made by turning the head. Blowflies can turn their head relative to the thorax around all three body axes but with different amplitudes (yaw, ±20°; pitch, ±20°; and roll, ±90°). Accordingly, movements of the thorax during flight are compensated for by countermovements of the head relative to the thorax (18-21). These head movements are mediated by the neck motor system, which consists of 21 pairs of muscles, with each of them innervated by a single motoneuron (22,23). The three oblique horizontal muscles, OH3-5, are supplied by the ventral cervical nerve, comprising the axons of three identical motor neurons, . Unilateral contraction of these muscles leads to a sidewise deflection of the head (yaw response), whereas bilateral contraction pulls th...

Flight Activity Alters Velocity Tuning of Fly Motion-Sensitive Neurons

“…Given how different the tasks of passively receiving a stimulus and active sensation are, it is not surprising that this assumption has been challenged more recently. Several pioneering studies, in vertebrates as well as insects, demonstrated that the behavioral state of an animal has a strong influence on sensory processing (Treue and Maunsell, 1996;Rind et al, 2008;Chiappe et al, 2010;Haag et al, 2010;Maimon et al, 2010;Niell and Stryker, 2010).…”

Elementary Motion Detection

“…While the increase in the firing rate after the application of CDM was about 3-fold, the increase associated with flying was about 6-10-fold. An increase in spontaneous activity is in accordance with work done in parallel on state-dependent influences of other lobula plate tangential cells in Drosophila and Calliphora Haag et al, 2010;Longden and Krapp, 2009;Longden and Krapp, 2010;Maimon et al, 2010;Rosner et al, 2010). In principle, four different behavioral states were investigated: application of CDM (Longden and Krapp, 2009), passive and active movement of the halteres Rosner et al, 2010), walking and flying (Maimon et al, 2010).…”

“…The other behavioral states are the flight condition and the CDM application condition. In the following I will compare the findings of this study with previous work (Heide, 1983) and recent literature on the effect of the behavioral state in flies Haag et al, 2010;Longden and Krapp, 2009;Longden and Krapp, 2010;Maimon et al, 2010;Rosner et al, 2010). Heide (1983) in collaboration with his colleagues Foster and McCann also recorded from a lobula plate tangential cell which they assumed to be H1.…”

“…Interestingly, the increase in baseline activity of H1 was rather weak (Rosner et al, 2010; fig and LPTC responses (Rosner et al, 2010;Haag et al, 2010). However, whereas argue that the observed baseline shift in HS cells is caused by backpropagation of activity from postsynaptic neurons via gap junction, Rosner et al (2010) assumed that the central signal is acting directly at the level of the lobula plate or presynaptically.…”

“…In insect neurobiology, the question of how behavior influences sensory processing has received more and more attention in recent years Haag et al, 2010;Maimon et al, 2010;Rind et al, 2008;Rosner et al, 2010). Using motion-sensitive (Schneider, 1953;Miller, 1977;Sandeman and Markl, 1980 (Rosner et al, 2010).…”