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Spatiotemporal and directional properties of visual neurons in the lentiformis mesencephali of the zebra finch and hummingbird Smyth, Graham


A moving animal experiences global visual signals across the entire retina known as optic flow, one of the key signals used in the visual guidance of locomotion. Optic flow sensitive neurons have been identified in the midbrains of all vertebrate classes. In birds, these neurons are found in the nucleus of the basal optic root (nBOR) and the pretectal nucleus lentiformis mesencephali (LM). These cells are known to exhibit large receptive fields in the contralateral eye, are excited by visual motion in a “preferred” direction and are inhibited by motion in the opposite direction. A key question is whether the response properties of LM neurons are conserved across species or are LM neurons specialized in animals that use different locomotor strategies. Previous studies in pigeons have investigated the responses of neurons in the LM and nBOR to drifting sine-wave gratings and discovered that they are tuned in the spatiotemporal domain. The LM typically contains cells that respond maximally to fast stimuli and are tuned to temporal frequency whereas nBOR cells respond maximally to slower stimuli and are velocity-tuned. Here we ask whether zebra finches and hummingbirds, specialized for different modes of locomotion, exhibit spatiotemporal specializations in optic flow neurons that may be related to their form of locomotion. We explored this question by making extracellular recordings in the LM of anesthetized birds while presenting drifting sine-wave gratings to the contralateral eye. These results were compared with previous pigeon data and we found that each of the three species exhibits distinct tuning in the spatiotemporal domain. Hummingbird LM neurons are tuned to the fastest stimuli, which were typically of lower spatial frequencies. Both hummingbird and finch LM cells exist almost exclusively as fast cells with 90% of peaks in the fast zone. Moreover, in pigeons, only ‘slow’ cells are velocity tuned, whereas both zebra finches and hummingbirds have ‘fast’ cells that are velocity tuned. These species-specific differences are suggestive of neural specializations for different optic flow behavior.

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