Organization and significance of neurons that detect change of visual depth in the hawk mothManduca sexta

Abstract

Visual stimuli representing looming or receding objects can be decomposed into four parameters: change in luminance; increase or decrease of area; increase or decrease of object perimeter length; and motion of the object's perimeter or edge. This paper describes intracellular recordings from visual neurons in the optic lobes of Manduca sexta that are selectively activated by certain of these parameters. Two classes of wide-field neurons have been identified that respond selectively to looming and receding stimuli. Class 1 cells respond to parameters of the image other than motion stimuli. They discriminate an approaching or receding disc from an outwardly or inwardly rotating spiral, being activated only by the disc and not by the spiral. Class 2 neurons respond to moving edges. They respond both to movement of the spiral and to an approaching or receding disc. These two classes are further subdivided into neurons that are excited by image expansion (looming) and are inhibited by image contraction (antilooming). Class 2 neurons also respond to horizontal and vertical movement of gratings over the retina. Stimulating class 1 and 2 neurons with white discs against a dark background results in the same activation as stimulation with dark discs against a white background, demonstrating that changes in luminance play no role in the detection of looming or antilooming. The present results show that the two types of looming-sensitive neurons in M. sexta use different mechanisms to detect the approach or retreat of an object. It is proposed that cardinal parameters for this are change of perimeter length detected by class 1 neurons and expansion or contraction visual flow fields detected by class 2 neurons. These two classes also differ with respect to their polarity, the former comprising centripetal cells from the optic lobes to the midbrain, the latter comprising centrifugal neurons from the midbrain to the optic lobes. The significance of these arrangements with respect to hovering flight is discussed.

Feedforward Inhibition Conveys Time-Varying Stimulus Information in a Collision Detection Circuit

“…We used 6 speeds varying from 7.1 to 227.2 °/s based on a characterization of LGMD speed tuning [35]. The width of the moving edge was ¼ of the width of the screen, like in the experiments described above.…”

Fuelling on the wing: sensory ecology of hawkmoth foraging

“…The neural control centres for vision, the optic lobes and the anterior optic tubercle, have been described in several species of hawkmoths, both in their coarse anatomy (for M. sexta , see el Jundi et al 2009 ; for M. stellatarum and D. elpenor , see; Stöckl et al 2016 ), and by the physiological responses of wide-field motion-sensitive neurons (e.g., Collett 1971 ; O’Carroll et al 1997 ; Kern 1998 ; Wicklein and Varjú 1999 ; Stöckl et al 2017b ) and looming-sensitive neurons (Wicklein and Strausfeld 2000 ) in the third optic neuropile, the lobula complex. The neurons that compute optic flow are crucial for flight control in insects (Borst 2014 ).…”

More than colour attraction: behavioural functions of flower patterns

“…Movement-derived visual information helps the insect to avoid collisions, negotiate narrow gaps, land on a surface, or locate the nest and foraging sites [recently viewed by 33 ]. Motion parallax and looming cues can improve the detection range for an object placed in front of a background [ 34 ], facilitate landing manoeuvres at flowers with shapes of distinct depths, or positioning of the proboscis [ 35 ].…”