Differential Tuning to Visual Motion Allows Robust Encoding of Optic Flow in the Dragonfly

Abstract

Visual cues provide an important means for aerial creatures to ascertain their self-motion through the environment. In many insects, including flies, moths, and bees, wide-field motion-sensitive neurons in the third optic ganglion are thought to underlie such motion encoding; however, these neurons can only respond robustly over limited speed ranges. The task is more complicated for some species of dragonflies that switch between extended periods of hovering flight and fast-moving pursuit of prey and conspecifics, requiring motion detection over a broad range of velocities. Since little is known about motion processing in these insects, we performed intracellular recordings from hawking, emerald dragonflies (Hemicordulia spp.) and identified a diverse group of motion-sensitive neurons that we named lobula tangential cells (LTCs). Following prolonged visual stimulation with drifting gratings, we observed significant differences in both temporal and spatial tuning of LTCs. Cluster analysis of these changes confirmed several groups of LTCs with distinctive spatiotemporal tuning. These differences were associated with variation in velocity tuning in response to translated, natural scenes. LTCs with differences in velocity tuning ranges and optima may underlie how a broad range of motion velocities are encoded. In the hawking dragonfly, changes in LTC tuning over time are therefore likely to support their extensive range of behaviors, from hovering to fast-speed pursuits.

Spike bursting in a dragonfly target-detecting neuron

“…This is observed when neurons are firing spikes in bursts, with multiple action potentials occurring in brief succession, followed by a prolonged period of inactivity. The ISIs of the other neurons exhibit a broad log-normal distribution, representative of spike rates observed in previous studies and indicative of non-bursting neurons 7 , 13 , 14 .…”

“…The lobula contains many STMD neurons, but three have been well-characterised; the centrifugal STMD, CSTMD1, and two binocular STMD neurons, BSTMD1 and BSTMD2 7 , 13 . Here we analyse recordings from these STMD neurons, as well as an ‘optic flow’ Lobula Tangential Cell 14 . Each STMD neuron is identified by its small target selectivity, characteristic receptive field and action potential waveform 5 , 7 , 13 CSTMD1 has a large receptive field with a sharp transition at the visual midline, with targets traversing the contralateral hemisphere with respect to our recording location driving inhibition and the ipsilateral driving strong excitation.…”

A Target-Detecting Visual Neuron in the Dragonfly Locks on to Selectively Attended Targets

“…The bimodal distribution of responses to paired-targets reveals the selection of either T 1 or T 2 . For comparison to a potential "null" hypothesis (i.e., no selective attention), Figure 2D shows results from a single lobula tangential cell in the dragonfly (Evans et al, 2019). This neuron generates robust responses using spatial summation to encode wide-field optic flow, analogous to lobula plate tangential cells in Diptera (Hausen, 1982).…”

The complex optic lobe of dragonflies

“…total brain volume, excluding the lamina = 6.81x10 8 µm 3 in Hemicordulia versus 6.95 x10 8 µm 3 in Manduca). We recently identified a diverse population of neurons in the dragonfly with similar physiological characteristics to LPTCs of other insects [33]. To investigate where these dragonfly lobula tangential cells (LTCs) lie in the dragonfly lobula complex, we combined intracellular recording techniques with fluorescent dye labelling ( fig.…”

“…Recordings obtained were during ongoing experiments aimed at classifying motion sensitive and feature selective neurons such as the small target motion detecting (STMD) neurons and lobula tangential cells (LTC's) described in our recent work [33,[39][40][41], from more than 300 dragonflies over a 4 year period. Upon establishing a healthy recording, all neurons were characterized using a range of stimuli presented on an LCD monitor (either an Eizo Foris FG2421 LCD at a frame rate of 120 Hz, or an Asus ROG Swift PG279Q IPS LCD at 165 Hz).…”