Octopaminergic modulation of contrast sensitivity

Abstract

Sensory systems adapt to prolonged stimulation by decreasing their response to continuous stimuli. Whereas visual motion adaptation has traditionally been studied in immobilized animals, recent work indicates that the animal's behavioral state influences the response properties of higher-order motion vision-sensitive neurons. During insect flight octopamine is released, and pharmacological octopaminergic activation can induce a fictive locomotor state. In the insect optic ganglia, lobula plate tangential cells (LPTCs) spatially pool input from local elementary motion detectors (EMDs) that correlate luminosity changes from two spatially discrete inputs after delaying the signal from one. The LPTC velocity optimum thereby depends on the spatial separation of the inputs and on the EMD's delay properties. Recently it was shown that behavioral activity increases the LPTC velocity optimum, with modeling suggesting this to originate in the EMD's temporal delay filters. However, behavior induces an additional post-EMD effect: the LPTC membrane conductance increases in flying flies. To physiologically investigate the degree to which activity causes presynaptic and postsynaptic effects, we conducted intracellular recordings of Eristalis horizontal system (HS) neurons. We constructed contrast response functions before and after adaptation at different temporal frequencies, with and without the octopamine receptor agonist chlordimeform (CDM). We extracted three motion adaptation components, where two are likely to be generated presynaptically of the LPTCs, and one within them. We found that CDM affected the early, EMD-associated contrast gain reduction, temporal frequency dependently. However, a CDM-induced change of the HS membrane conductance disappeared during and after visual stimulation. This suggests that physical activity mainly affects motion adaptation presynaptically of LPTCs, whereas post-EMD effects have a minimal effect.

Octopaminergic modulation of the visual flight speed regulator ofDrosophila

“…2B), resulting in a vastly more complex network of modulation than accounted for by either the H1 or H2 models. In addition to its role in the LPTC network, octopamine has been implicated in modulation of contrast sensitivity and motion adaptation in visual processing presynaptic to the LPTC network, presumably within the elementary motion detection circuits (de Haan et al, 2012). Because contrast has been shown to influence baseline flight speed (Straw et al, 2011), octopamine could have an indirect influence on a flies' preferred visual set point, which could also explain the slight increase in baseline flight speed that we observed.…”

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow

“…Several recent studies have concordantly shown that locomotor activity as well as systemic administration of octopamine or its agonist CDM elevates the resting activity of fly LPTCs and enhances their stimulus-induced responses (Longden and Krapp, 2009, 2010; Chiappe et al, 2010; Maimon et al, 2010; Jung et al, 2011; Haan et al, 2012; Rien et al, 2012; Suver et al, 2012). In some of these studies, the response boost was particularly strong at high temporal frequencies of grating motion (Chiappe et al, 2010; Longden and Krapp, 2010; Jung et al, 2011).…”

“…Mutant flies lacking the enzyme for the synthesis of octopamine from its precursor tyramine are impaired in flight initiation and maintenance (Brembs et al, 2007). In flies as well as in locusts, administration of octopamine or its agonist chlordimeform (CDM) was shown to affect visual processing (Bacon et al, 1995; Longden and Krapp, 2009, 2010; Jung et al, 2011; Haan et al, 2012; Rien et al, 2012). …”

A decision underlies phototaxis in an insect

“…However, recent research has shown that many of these behaviours are either more complex than initially imagined [16–19] or liable to exploitation [20]. Moreover, several studies have shown that the state of the animal modulates how sensory structures process identical stimuli [21–26] and many of these modulations are caused by aminergic actions [1,2,21,27–29]. Owing to observations like these, the general concept of behaviours as responses to external stimuli (sensorimotor hypothesis) has come under ever more critical scrutiny in the last decade.…”