Encoding of Yaw in the Presence of Distractor Motion: Studies in a Fly Motion Sensitive Neuron

Abstract

Motion estimation is crucial for aerial animals such as the fly, which perform fast and complex maneuvers while flying through a 3-D environment. Motion-sensitive neurons in the lobula plate, a part of the visual brain, of the fly have been studied extensively for their specialized role in motion encoding. However, the visual stimuli used in such studies are typically highly simplified, often move in restricted ways, and do not represent the complexities of optic flow generated during actual flight. Here, we use combined rotations about different axes to study how H1, a wide-field motion-sensitive neuron, encodes preferred yaw motion in the presence of stimuli not aligned with its preferred direction. Our approach is an extension of "white noise" methods, providing a framework that is readily adaptable to quantitative studies into the coding of mixed dynamic stimuli in other systems. We find that the presence of a roll or pitch ("distractor") stimulus reduces information transmitted by H1 about yaw, with the amount of this reduction depending on the variance of the distractor. Spike generation is influenced by features of both yaw and the distractor, where the degree of influence is determined by their relative strengths. Certain distractor features may induce bidirectional responses, which are indicative of an imbalance between global excitation and inhibition resulting from complex optic flow. Further, the response is shaped by the dynamics of the combined stimulus. Our results provide intuition for plausible strategies involved in efficient coding of preferred motion from complex stimuli having multiple motion components.

The impulse response of optic flow-sensitive descending neurons to roll m-sequences

“…For example, the blowfly H1 neuron's spike-triggered average to yaw, roll and pitch has a time to peak (TTP) of ca. 20 ms, and a slow return to baseline after about 100 ms (Roy et al, 2015). In addition, the yaw spike-triggered average is decreased in amplitude by the addition of either roll or pitch (Roy et al, 2015).…”

“…In blowflies, the yaw spike-triggered average in H1 neurons is affected by the addition of either roll or pitch (Roy et al, 2015). To investigate whether the roll impulse response in optic flow-sensitive descending neurons is affected by constant optic flow, we added inihibitory or excitatory roll at 25 or 50 deg s −1 to Roll 33 m-sequences (Movies 2 and 3).…”

“…20 ms, and a slow return to baseline after about 100 ms (Roy et al, 2015). In addition, the yaw spike-triggered average is decreased in amplitude by the addition of either roll or pitch (Roy et al, 2015). The Drosophila HS cell impulse response to sinusoidal gratings controlled by an m-sequence also peaks early, and then decays back to baseline in less than 400 ms, following an exponential decay with a time constant of 65 ms (Schnell et al, 2014).…”

“…One way to study optic flow sensitivity is to use white noise techniques (Ringach and Shapley, 2004;Roy et al, 2015). Whitenoise stimuli are powerful in that they comparatively rapidly provide the data needed to extract the spatio-temporal response dynamics of a neuron or a visual behavior.…”

“…To understand more about the spatio-temporal dynamics of these neurons, we thus extracted the impulse response to m-sequences controlling roll motion. As the H1 yaw spike-triggered average has been shown to be affected by the addition of other types of optic flow (Roy et al, 2015), we additionally quantified the roll impulse response after adding constant roll or lift motion, and found that the roll impulse response was strongly affected by this.…”