Monitoring of Single-Cell Responses in the Optic Tectum of Adult Zebrafish with Dextran-Coupled Calcium Dyes Delivered via Local Electroporation

Kassing V, Engelmann J, Kurtz R. Monitoring of Single-Cell Responses in the Optic Tectum of Adult Zebrafish with Dextran-Coupled Calcium Dyes Delivered via Local Electroporation. PLoS ONE. 2013;8(5): e62846.The zebrafish (Danio rerio) has become one of the major animal models for in vivo examination of sensory and neuronal computation. Similar to Xenopus tadpoles neural activity in the optic tectum, the major region controlling visually guided behavior, can be examined in zebrafish larvae by optical imaging. Prerequisites of these approaches are usually the transparency of larvae up to a certain age and the use of two-photon microscopy. This principle of fluorescence excitation was necessary to suppress crosstalk between signals from individual neurons, which is a critical issue when using membrane-permeant dyes. This makes the equipment to study neuronal processing costly and limits the approach to the study of larvae. Thus there is lack of knowledge about the properties of neurons in the optic tectum of adult animals. We established a procedure to circumvent these problems, enabling in vivo calcium imaging in the optic tectum of adult zebrafish. Following local application of dextran-coupled dyes single-neuron activity of adult zebrafish can be monitored with conventional widefield microscopy, because dye labeling remains restricted to tens of neurons or less. Among the neurons characterized with our technique we found neurons that were selective for a certain pattern orientation as well as neurons that responded in a direction-selective way to visual motion. These findings are consistent with previous studies and indicate that the functional integrity of neuronal circuits in the optic tectum of adult zebrafish is preserved with our staining technique. Overall, our protocol for in vivo calcium imaging provides a useful approach to monitor visual responses of individual neurons in the optic tectum of adult zebrafish even when only widefield microscopy is available. This approach will help to obtain valuable insight into the principles of visual computation in adult vertebrates and thus complement previous work on developing visual circuits

Visuomotor Transformation in the Fly Gaze Stabilization System

For sensory signals to control an animal's behavior, they must first be transformed into a format appropriate for use by its motor systems. This fundamental problem is faced by all animals, including humans. Beyond simple reflexes, little is known about how such sensorimotor transformations take place. Here we describe how the outputs of a well-characterized population of fly visual interneurons, lobula plate tangential cells (LPTCs), are used by the animal's gaze-stabilizing neck motor system. The LPTCs respond to visual input arising from both self-rotations and translations of the fly. The neck motor system however is involved in gaze stabilization and thus mainly controls compensatory head rotations. We investigated how the neck motor system is able to selectively extract rotation information from the mixed responses of the LPTCs. We recorded extracellularly from fly neck motor neurons (NMNs) and mapped the directional preferences across their extended visual receptive fields. Our results suggest that—like the tangential cells—NMNs are tuned to panoramic retinal image shifts, or optic flow fields, which occur when the fly rotates about particular body axes. In many cases, tangential cells and motor neurons appear to be tuned to similar axes of rotation, resulting in a correlation between the coordinate systems the two neural populations employ. However, in contrast to the primarily monocular receptive fields of the tangential cells, most NMNs are sensitive to visual motion presented to either eye. This results in the NMNs being more selective for rotation than the LPTCs. Thus, the neck motor system increases its rotation selectivity by a comparatively simple mechanism: the integration of binocular visual motion information

Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action

Egelhaaf M, Boeddeker N, Kern R, Kurtz R, Lindemann JP. Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action. Frontiers in Neural Circuits. 2012;6:108.Insects such as flies or bees, with their miniature brains, are able to control highly aerobatic flight maneuvres and to solve spatial vision tasks, such as avoiding collisions with obstacles, landing on objects, or even localizing a previously learnt inconspicuous goal on the basis of environmental cues. With regard to solving such spatial tasks, these insects still outperform man-made autonomous flying systems. To accomplish their extraordinary performance, flies and bees have been shown by their characteristic behavioral actions to actively shape the dynamics of the image flow on their eyes ("optic flow"). The neural processing of information about the spatial layout of the environment is greatly facilitated by segregating the rotational from the translational optic flow component through a saccadic flight and gaze strategy. This active vision strategy thus enables the nervous system to solve apparently complex spatial vision tasks in a particularly efficient and parsimonious way. The key idea of this review is that biological agents, such as flies or bees, acquire at least part of their strength as autonomous systems through active interactions with their environment and not by simply processing passively gained information about the world. These agent-environment interactions lead to adaptive behavior in surroundings of a wide range of complexity. Animals with even tiny brains, such as insects, are capable of performing extraordinarily well in their behavioral contexts by making optimal use of the closed action-perception loop. Model simulations and robotic implementations show that the smart biological mechanisms of motion computation and visually-guided flight control might be helpful to find technical solutions, for example, when designing micro air vehicles carrying a miniaturized, low-weight on-board processor

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

Rien D, Kern R, Kurtz R. Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow. Frontiers in Behavioral Neuroscience. 2013;7:155.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

Octopaminergic modulation of temporal frequency tuning of a fly visual motion-sensitive neuron depends on adaptation level

Lüders J, Kurtz R. Octopaminergic modulation of temporal frequency tuning of a fly visual motion-sensitive neuron depends on adaptation level. Frontiers in Integrative Neuroscience. 2015;9: 36.Several recent studies in invertebrates as well as vertebrates have demonstrated that neuronal response characteristics of sensory neurons can be profoundly affected by an animal’s locomotor activity. The functional consequences of such state-dependent modulation have been a matter of intense debate. In flies, a particularly interesting finding was that tethered walking or flying causes not only general response enhancement of visual motion-sensitive neurons, but also broadens their temporal frequency tuning towards higher values. However, in other studies such state-dependent alterations of neuronal tuning functions were not found. We hypothesize that these discrepancies were due to different adaptation levels of the motion-sensitive neurons, resulting from the use of different stimulation protocols. This is plausible, because the strength of adaptation during ongoing stimulation was shown to be affected by chlordimeform (CDM), an agonist of the insect neuromodulator octopamine, which mediates state-dependent modulation. Our results show that CDM causes broadening of the temporal frequency tuning of the blowfly’s visual motion-sensitive H1 neuron only in the adapted state, but not prior to the presentation of adapting motion. Thus, our study indicates that seemingly conflicting results on the locomotor state-dependence of neuronal tuning functions are consistent when considering the neurons’ adaptation level. Moreover, it demonstrates that stimulation history has to be considered when the significance of state-dependent modulation of sensory processing is interpreted

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

Rien D, Kern R, Kurtz R. Synaptic transmission of graded membrane potential changes and spikes between identified visual interneurons. European Journal of Neuroscience. 2011;34(5):705-716

Spatiotemporal Processing of Dynamic Visual Information in the Insect Neural System

Kurtz R. Spatiotemporal Processing of Dynamic Visual Information in the Insect Neural System. In: DiLorenzo P, Victor J, eds. Spike Timing: Mechanism and Function. Frontiers in Neuroscience. 1st ed. Boca Raton: CRC Press; 2013: 1-24