Facilitation of dragonfly target-detecting neurons by slow moving features on continuous paths

Abstract

Dragonflies detect and pursue targets such as other insects for feeding and conspecific interaction. They have a class of neurons highly specialized for this task in their lobula, the “small target motion detecting” (STMD) neurons. One such neuron, CSTMD1, reaches maximum response slowly over hundreds of milliseconds of target motion. Recording the intracellular response from CSTMD1 and a second neuron in this system, BSTMD1, we determined that for the neurons to reach maximum response levels, target motion must produce sequential local activation of elementary motion detecting elements. This facilitation effect is most pronounced when targets move at velocities slower than what was previously thought to be optimal. It is completely disrupted if targets are instantaneously displaced a few degrees from their current location. Additionally, we utilize a simple computational model to discount the parsimonious hypothesis that CSTMD1's slow build-up to maximum response is due to it incorporating a sluggish neural delay filter. Whilst the observed facilitation may be too slow to play a role in prey pursuit flights, which are typically rapidly resolved, we hypothesize that it helps maintain elevated sensitivity during prolonged, aerobatically intricate conspecific pursuits. Since the effect seems to be localized, it most likely enhances the relative salience of the most recently “seen” locations during such pursuit flights.

Correlation between OFF and ON Channels Underlies Dark Target Selectivity in an Insect Visual System

“…These include the ability to selectively attend to a single target in the presence of a distractor (Wiederman and O'Carroll, 2013b), as well as exhibiting a slow facilitation of its response for targets that move along a continuous trajectory (Nordström at al. 2011;Dunbier et al, 2012). However, CSTMD1 is a neuron that responds very quickly in absolute terms, with a response latency Ͻ50 ms (Nordström et al, 2011) and tuning to high target velocity (Geurten et al, 2007;Dunbier et al, 2012).…”

“…Although we previously suggested this provides evidence for an HR-EMD framework, the result is also consistent with an ESTMD correlation model. There is a pronounced velocity optimum that would be determined by early visual filtering and the correlation delay time constant (Geurten et al, 2007;Dunbier et al, 2012), with the optimum velocity increasing as target width increases in the direction of travel (Geurten et al, 2007). This is the result of the increased spatial separation between the leading and trailing edge of the target, requiring a faster transit speed to match a given delay between OFF and ON channels.…”

“…However, CSTMD1 is a neuron that responds very quickly in absolute terms, with a response latency Ͻ50 ms (Nordström et al, 2011) and tuning to high target velocity (Geurten et al, 2007;Dunbier et al, 2012). Our modeling of its response kinetics suggests that the facilitation must be the result of a higher-order property within the STMD pathway (e.g., attentional modulation) in response to slower moving features, rather than any inherent sluggishness in the time constants of the underlying motion pathway (Dunbier et al, 2011(Dunbier et al, , 2012. Thus, some caution is still in order in attributing the observed supralinear response characteristics of CSTMD1 to an underlying elementary correlation between local OFF and ON channels, versus a mechanism that upregulates attention for the highly salient target stimulus.…”

“…2011;Dunbier et al, 2012). However, CSTMD1 is a neuron that responds very quickly in absolute terms, with a response latency Ͻ50 ms (Nordström et al, 2011) and tuning to high target velocity (Geurten et al, 2007;Dunbier et al, 2012). Our modeling of its response kinetics suggests that the facilitation must be the result of a higher-order property within the STMD pathway (e.g., attentional modulation) in response to slower moving features, rather than any inherent sluggishness in the time constants of the underlying motion pathway (Dunbier et al, 2011(Dunbier et al, , 2012.…”

“…1A) have previously been used to model spatiotemporal tuning of STMD neurons (Geurten et al, 2007;Dunbier et al, 2011Dunbier et al, , 2012, these models lack the size selectivity that characterizes STMDs. We therefore previously proposed the ESTMD (Fig.…”