Function and Coding in the Blowfly H1 Neuron during Naturalistic Optic Flow

Abstract

Naturalistic stimuli, reconstructed from measured eye movements of flying blowflies, were replayed on a panoramic stimulus device. The directional movement-sensitive H1 neuron was recorded from blowflies watching these stimuli. The response of the H1 neuron is dominated by the response to fast saccadic turns into one direction. The response between saccades is mostly inhibited by the front-toback optic flow caused by the forward translation during flight. To unravel the functional significance of the H1 neuron, we replayed, in addition to the original behaviorally generated stimulus, two targeted stimulus modifications: (1) a stimulus in which flow resulting from translation was removed (this stimulus produced strong intersaccadic responses); and (2) a stimulus in which the saccades were removed by assuming that the head follows the smooth flight trajectory (this stimulus produced alternating zero or nearly saturating spike rates). The responses to the two modified stimuli are strongly different from the response to the original stimulus, showing the importance of translation and saccades for the H1 response to natural optic flow. The response to the original stimulus thus suggests a double function for the H1 neuron, assisting two major classes of movement-sensitive output neurons targeted by H1. First, its strong response to saccades may function as a saccadic suppressor (via one of its target neurons) for cells involved in figure-ground discrimination. Second, its intersaccadic response may increase the signal-to-noise ratio (SNR) of wide-field neurons involved in detecting translational optic flow between saccades, in particular when flying speeds are low or when object distances are large.

Responses of blowfly motion-sensitive neurons to reconstructed optic flow along outdoor flight paths

“…5e, f). The response of the neuron thus reflects the animal's rotational velocity in a highly non-linear fashion (Egelhaaf and Reichardt 1987;Haag and Borst 1997;Kern et al 2001b;van Hateren et al 2005).…”

“…In the present study these responses to translational optic flow are more pronounced, presumably because the speed of flying flies is much higher than that of walking flies. When HSE-Cells are confronted with the optic flow reconstructed from free flight manoeuvres the time course of the response is not proportional to the time course of the fly's rotational velocity, which casts doubt on the common view that the HSE-cell acts primarily as a rotation detector (Kern et al 2005b;Lindemann et al 2003bLindemann et al , 2005van Hateren et al 2005). These studies also show that HSE responses can provide information about translation and thus, implicitly, about the spatial relation of the animal to its surroundings during the intervals between saccades.…”

“…Our results corroborate the point that differences in the appearance of natural scenes have little effect on the responses of fly motion sensitive neurons, but they also show that the dynamical properties of the behaviourally generated optic flow strongly influence the neuronal responses. This aspect has been stressed by several recent studies, which analysed the performance of identified neurons in the visual system of the fly by confronting them with image sequences as they are experienced during walking and flight in indoor environments with a 3-D structure Kern et al 2000Kern et al , 2001bKern et al , 2005bKimmerle and Egelhaaf 2000a, b;Lindemann et al 2003bLindemann et al , 2005van Hateren et al 2005;Egelhaaf 1996, 1997). During walking, the response of the HSE-Cell does reflect the animal's turning direction nearly independently of the texture and spatial layout of the environment, but is also affected by translational flow when the animal walks close to objects (Kern et al 2001a, b).…”

“…Three identified TCs of the horizontal system (HS) in each hemisphere of the blowfly brain respond in a directionally selective manner to horizontal visual motion, as it occurs for instance during rotations about the vertical (yaw) axis (Hausen 1982a, b). When optic flow as experienced in free flight is replayed to HScells the neuronal signals provide information on translational self-motion between saccades and thus, implicitly, on the spatial relation of the animal to its environment (Kern et al 2005b;Lindemann et al 2005;van Hateren et al 2005). This evidence indicates that, in contrast to previous conclusions (e.g.…”

“…However, the reconstruction of natural optic flow has so far been restricted to space-confined indoor flight cages (Kern et al 2001b(Kern et al , 2005bLindemann et al 2003b;van Hateren et al 2005) which, on the one hand, make it possible to reconstruct flight paths and head orientation with high precision, but on the other hand lack a number of properties of outdoors scenes: (1) natural scenes can contain objects at all distances, from close-by to infinity, which results in a patchy and sparse distribution of translational optic flow (Zanker and Zeil 2005); (2) objects, textures and contrast can be distributed very unequally in different viewing directions; (3) natural scenes can contain significant environmental background motion, generated for instance by wind-driven vegetation.…”