Object representation and distance encoding in three-dimensional environments by a neural circuit in the visual system of the blowfly

Abstract

Three motion-sensitive key elements of a neural circuit, presumably involved in processing object and distance information, were analyzed with optic flow sequences as experienced by blowflies in a three-dimensional environment. This optic flow is largely shaped by the blowfly's saccadic flight and gaze strategy, which separates translational flight segments from fast saccadic rotations. By modifying this naturalistic optic flow, all three analyzed neurons could be shown to respond during the intersaccadic intervals not only to nearby objects but also to changes in the distance to background structures. In the presence of strong background motion, the three types of neuron differ in their sensitivity for object motion. Object-induced response increments are largest in FD1, a neuron long known to respond better to moving objects than to spatially extended motion patterns, but weakest in VCH, a neuron that integrates wide-field motion from both eyes and, by inhibiting the FD1 cell, is responsible for its object preference. Small but significant object-induced response increments are present in HS cells, which serve both as a major input neuron of VCH and as output neurons of the visual system. In both HS and FD1, intersaccadic background responses decrease with increasing distance to the animal, although much more prominently in FD1. This strong dependence of FD1 on background distance is concluded to be the consequence of the activity of VCH that dramatically increases its activity and, thus, its inhibitory strength with increasing distance.

Gaze characteristics of freely walking blowflies in a goal-directed task

“…(2) Besides detection of self-movement (Krapp, 2000), LPTCs are thought to be involved in spatial vision by extracting distances from translational optic flow during intersaccadic intervals in free-flying flies Karmeier et al, 2006;Kern et al, 2005;Kern et al, 2006;Liang et al, 2008;Liang et al, 2011;Liang et al, 2012). Because stride-coupled rotations are likely to affect the responses of LPTCs, they might impair the acquisition of spatial information.…”

“…Candidate neurons that might be involved are LPTCs, such as the figure detecting cells (FD cells) (Egelhaaf, 1985a;Egelhaaf, 1985b;Liang et al, 2012) and the LPTCs, which have already been mentioned, that are most sensitive to wide-field motion. However, the most challenging demand for a network comparing edge velocities is the assignment of the corresponding edges to an object, especially in the presence of multiple objects and background structures in the environment.…”

Impact of stride-coupled gaze shifts of walking blowflies on the neuronal representation of visual targets

“…Retinal bar expansion velocity increases with increasing nearness of the fly to the bar and might thus be extracted by comparing the retinal velocity of the bar’s right and left edges (Kress and Egelhaaf, 2014). Here, we tested to what extent this simple computation might be approximated by comparing the responses of the ipsi- and contralateral HSE cells, which are known to represent nearness information about objects during intersaccadic flight phases (Kern et al, 2005; Karmeier et al, 2006; Liang et al, 2008, 2012). …”

“…To reconstruct the visual input encountered by the freely walking flies during the approach to the bar, we combined the fly’s head position and orientation (Figure 1B), the respective position of the bar and the background on the projection screen as well as the interior appearance of the walking arena (Figure 1A) in a computer model created in Open Inventor 1 . These data were used to render the ego-perspective stimulus movies presented on our panoramic LED arena, FliMax (for more information about the rendering procedure see: Lindemann et al, 2003; Geurten et al, 2012; Liang et al, 2012). The stimuli were either shaped exclusively by self-induced image shifts (stationary stimulus condition) or a combination of self-produced and external motion cues of the bar (moving bar condition) or of the textured background (moving background condition).…”

“…This property as well as the finding that they directly project to the head motor system, suggest that LPTCs could play a fundamental role in the above described gaze compensation (Strausfeld and Seyan, 1985; Milde and Strausfeld, 1986; Huston and Krapp, 2008, 2009; Haag et al, 2010; Wertz et al, 2012). Moreover, LPTCs sensitive to horizontal motion have been concluded to extract distance information from the image motion caused by translational self-motion during flight (Kern et al, 2005; Karmeier et al, 2006; Liang et al, 2008, 2012; review: Egelhaaf et al, 2012). …”