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

Visual stimuli representing looming or receding objects can be decomposed i nto four parameters: change in luminance; increase or decrease of area; inc rease or decrease of object perimeter length; and motion of the object's pe rimeter 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. C lass 2 neurons respond to moving edges. They respond both to movement of th e spiral and to an approaching or receding disc. These two classes are furt her subdivided into neurons that are excited by image expansion (looming) a nd are inhibited by image contraction (antilooming). Class 2 neurons also r espond to horizontal and vertical movement of gratings over the retina. Sti mulating class 1 and 2 neurons with white discs against a dark background r esults in the same activation as stimulation with dark discs against a whit e background, demonstrating that changes in luminance play no role in the d etection of looming or antilooming. The present results show that the two t ypes of looming-sensitive neurons in M. sexta use different mechanisms to d etect the approach or retreat of an object. It is proposed that cardinal pa rameters for this are change of perimeter length detected by class 1 neuron s and expansion or contraction visual flow fields detected by class 2 neuro ns. These two classes also differ with respect to their polarity, the forme r comprising centripetal cells from the optic lobes to the midbrain, the la tter comprising centrifugal neurons from the midbrain to the optic lobes. T he significance of these arrangements with respect to hovering flight is di scussed. J. Comp. Neurol. 424:356-376, 2000. (C) 2000 Wiley-Liss, Inc.