Electrophysiological Method for Recording Intracellular Voltage Responses of <em>Drosophila</em> Photoreceptors and Interneurons to Light Stimuli <em>In Vivo</em>

Voltage responses of insect photoreceptors and visual interneurons can be accurately recorded with conventional sharp microelectrodes. The method ...

Beijing Normal University

The University of Sheffield

Several physiological mechanisms allow sensory information to be propagated in neuronal networks. According to the conventional view of signal processing, graded changes of membrane potential at the dendrite are converted into a sequence of spikes. However, in many sensory receptors and several types of mostly invertebrate neurons, graded potential changes have a direct impact on the cells' output signals. The visual system of the blowfly Calliphora vicina is a good model system to study synaptic transmission in vivo during sensory stimulation. We recorded extracellularly from an identified motion-sensitive neuron while simultaneously measuring and controlling the membrane potential of individual elements of its presynaptic input ensemble. The membrane potential in the terminals of the presynaptic neuron is composed of two components, graded membrane potential changes and action potentials. To dissociate the roles of action potentials and graded potential changes in synaptic transmission we used voltage-clamp-controlled current-clamp techniques to suppress the graded membrane potential changes without affecting action potentials. Our results indicate that both the graded potential and the action potentials of the presynaptic neuron have an impact on the spiking characteristics of the postsynaptic neuron. Although a tight temporal coupling between pre- and postsynaptic spikes exists, the timing between these spikes is also affected by graded potential changes. We propose that the control of synaptic transfer of a dynamically complex signal by graded changes in membrane potential and spikes is useful to enable a temporally precise coupling of spikes in response to sudden transitions in stimulus intensity.

Synaptic transmission of graded membrane potential changes and spikes between identified visual interneurons.

Locomotor activity like walking or flying has recently been shown to alter visual processing in several species. In insects, the neuromodulator octopamine is thought to play an important role in mediating state changes during locomotion of the animal [K.D. Longden & H.G. Krapp (2009) J. Neurophysiol., 102, 3606-3618; (2010) Front. Syst. Neurosci., 4, 153; S.N. Jung et al. (2011)J. Neurosci., 31, 9231-9237]. Here, we used the octopamine agonist chlordimeform (CDM) to mimic effects of behavioural state changes on visual motion processing. We recorded from identified motion-sensitive visual interneurons in the lobula plate of the blowfly Calliphora vicina. In these neurons, which are thought to be involved in visual guidance of locomotion, motion adaptation leads to a prominent attenuation of contrast sensitivity. Following CDM application, the neurons maintained high contrast sensitivity in the adapted state. This modulation of contrast gain adaptation was independent of the activity of the recorded neurons, because it was also present after stimulation with visual motion that did not result in deviations from the neurons' resting activity. We conclude that CDM affects presynaptic inputs of the recorded neurons. Accordingly, the effect of CDM was weak when adapting and test stimuli were presented in different parts of the receptive field, stimulating separate populations of local presynaptic neurons. In the peripheral visual system adaptation depends on the temporal frequency of the stimulus pattern and is therefore related to pattern velocity. Contrast gain adaptation could therefore be the basis for a shift in the velocity tuning that was previously suggested to contribute to state-dependent processing of visual motion information in the lobula plate interneurons.

Octopaminergic modulation of contrast gain adaptation in fly visual motion-sensitive neurons.

In a variety of species locomotor activity, like walking or flying, has been demonstrated to alter visual information processing. The neuromodulator octopamine was shown to change the response characteristics of optic flow processing neurons in the fly's visual system in a similar way as locomotor activity. This modulation resulted in enhanced neuronal responses, in particular during sustained stimulation with high temporal frequencies, and in shorter latencies of responses to abrupt onsets of pattern motion. These state-dependent changes were interpreted to adjust neuronal tuning to the range of high velocities encountered during locomotion. Here we assess the significance of these changes for the processing of optic flow as experienced during flight. Naturalistic image sequences were reconstructed based on measurements of the head position and gaze direction of Calliphora vicina flying in an arena. We recorded the responses of the V1 neuron during presentation of these image sequences on a panoramic stimulus device ("FliMax"). Consistent with previous accounts, we found that spontaneous as well as stimulus-induced spike rates were increased by an octopamine agonist and decreased by an antagonist. Moreover, a small but consistent decrease in response latency upon octopaminergic activation was present, which might support fast responses to optic flow cues and limit instabilities during closed-loop optomotor regulation. However, apart from these effects the similarities between the dynamic response properties in the different pharmacologically induced states were surprisingly high, indicating that the processing of naturalistic optic flow is not fundamentally altered by octopaminergic modulation.

Diana Rien

National Key Laboratory of Cognitive Neuroscience and Learning

Beijing Normal University

Electrophysiological Method for Recording Intracellular Voltage Responses of Drosophila Photoreceptors and Interneurons to Light Stimuli In Vivo

Diana Rien

.css-o250i3{font-size:18px;font-family:Open Sans,sans-serif;line-height:21.6px;}National Key Laboratory of Cognitive Neuroscience and Learning

Beijing Normal University

Electrophysiological Method for Recording Intracellular Voltage Responses of Drosophila Photoreceptors and Interneurons to Light Stimuli In Vivo

National Key Laboratory of Cognitive Neuroscience and Learning