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Non-canonical Receptive Field Properties and Neuromodulation of Feature-Detecting Neurons in Flies.

ABSTRACT: Several fundamental aspects of motion vision circuitry are prevalent across flies and mice. Both taxa segregate ON and OFF signals. For any given spatial pattern, motion detectors in both taxa are tuned to speed, selective for one of four cardinal directions, and modulated by catecholamine neurotransmitters. These similarities represent conserved, canonical properties of the functional circuits and computational algorithms for motion vision. Less is known about feature detectors, including how receptive field properties differ from the motion pathway or whether they are under neuromodulatory control to impart functional plasticity for the detection of salient objects from a moving background. Here, we investigated 19 types of putative feature selective lobula columnar (LC) neurons in the optic lobe of the fruit fly Drosophila melanogaster to characterize divergent properties of feature selection. We identified LC12 and LC15 as feature detectors. LC15 encodes moving bars, whereas LC12 is selective for the motion of discrete objects, mostly independent of size. Neither is selective for contrast polarity, speed, or direction, highlighting key differences in the underlying algorithms for feature detection and motion vision. We show that the onset of background motion suppresses object responses by LC12 and LC15. Surprisingly, the application of octopamine, which is released during flight, reverses the suppressive influence of background motion, rendering both LCs able to track moving objects superimposed against background motion. Our results provide a comparative framework for the function and modulation of feature detectors and new insights into the underlying neuronal mechanisms involved in visual feature detection.

SUBMITTER: Stadele C

PROVIDER: S-EPMC7343589 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Extrastriate area V4 is a critical component of visual form processing in both humans and non-human primates. Previous studies have shown that the tuning properties of V4 neurons demonstrate an intermediate level of complexity that lies between the narrow band orientation and spatial frequency tuning of neurons in primary visual cortex and the highly complex object selectivity seen in inferotemporal neurons. However, the nature of feature selectivity within this cortical area is not well understood, especially in the context of natural stimuli. Specifically, little is known about how the tuning properties of V4 neurons, measured in isolation, translate to feature selectivity within natural scenes. In this study, we assessed the degree to which preferences for natural image components can readily be inferred from classical orientation and spatial frequency tuning functions. Using a psychophysically-inspired method we isolated and identified the specific visual "driving features" occurring in natural scene photographs that reliably elicited spiking activity from single V4 neurons. We then compared the measured driving features to those predicted based on the spectral receptive field (SRF), estimated from responses to narrowband sinusoidal grating stimuli. This approach provided a quantitative framework for assessing the degree to which linear feature selectivity was preserved during natural vision. First, we found evidence of both spectrally and spatially tuned suppression within the receptive field, neither of which were present in the linear SRF. Second, we found driving features that were stable during translation of the image across the receptive field (due to small fixational eye movements). The degree of translation invariance fell along a continuum, with some cells showing nearly complete invariance across the receptive field and others exhibiting little to no position invariance. This form of limited translation invariance could indicate that a subset of V4 neurons are insensitive to small fixational eye movements, supporting perceptual stability during natural vision.

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Non-canonical Receptive Field Properties and Neuromodulation of Feature-Detecting Neurons in Flies.

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