Dynamic modulation of visual and electrosensory gains for locomotor control

Sutton, Erin E.; Demir, Alican; Stamper, Sarah A.; Fortune, Eric S.; Cowan, Noah J.

doi:10.1098/rsif.2016.0057

Cited by 26 publications

(28 citation statements)

References 41 publications

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“…This is consistent with studies on mammalian species (such as humans, monkeys and rats) that reveal that sensory inputs are weighted, which often leads to a dominance of certain senses during particular situations and tasks3456. These results are consistent with studies in South American weakly electric fish (Gymnotidae), which also showed a dominance of the electric sense over vision during refuge-tracking and object discrimination3031.…”

Section: Discussionsupporting

confidence: 89%

Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fish Gnathonemus petersii

Schumacher

Perera

Emde

2017

Sci Rep

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Animal multisensory systems are able to cope with discrepancies in information provided by individual senses by integrating information using a weighted average of the sensory inputs. Such sensory weighting often leads to a dominance of a certain sense during particular tasks and conditions, also called sensory capture. Here we investigated the interaction of vision and active electrolocation during object discrimination in the weakly electric fish Gnathonemus petersii. Fish were trained to discriminate between two objects using both senses and were subsequently tested using either only vision or only the active electric sense. We found that at short range the electric sense dominates over vision, leading to a decreased ability to discriminate between objects visually when vision and electrolocation provide conflicting information. In line with visual capture in humans, we call this dominance of the electric sense electrosensory capture. Further, our results suggest that the fish are able to exploit the advantages of multiple senses using vision and electrolocation redundantly, synergistically and complementarily. Together our results show that by providing similar information about the environment on different spatial scales, vision and the electric sense of G. petersii are well attuned to each other producing a robust and flexible percept.

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Section: Discussionsupporting

confidence: 89%

Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fish Gnathonemus petersii

Schumacher

Perera

Emde

2017

Sci Rep

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“…The time constant of this decay was similar to the value we obtained by fitting our model. Summation of cues from different modalities has been proposed previously to explain stabilization reflexes [34,35] and forward velocity control [26,36,37] in flies and fish. Summation of visual and odor information has been observed in turning behavior of tethered flies [38], and in the turn probability of freely moving larvae [7].…”

Section: Discussionmentioning

confidence: 99%

Multisensory Control of Orientation in Tethered Flying Drosophila

Currier

Nagel

2018

Current Biology

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Summary A longstanding goal of systems neuroscience is to quantitatively describe how the brain integrates sensory cues over time. Here we develop a closed-loop orienting paradigm in Drosophila to study the algorithms by which cues from two modalities are integrated during ongoing behavior. We find that flies exhibit two behaviors when presented simultaneously with an attractive visual stripe and aversive wind cue. First, flies perform a turn sequence where they initially turn away from the wind and but later turn back toward the stripe, suggesting dynamic sensory processing. Second, turns toward the stripe are slowed by the presence of competing wind, suggesting summation of turning drives. We develop a model in which signals each modality are filtered in space and time to generate turn commands, then summed to produce ongoing orienting behavior. This computational framework correctly predicts behavioral dynamics for a range of stimulus intensities and spatial arrangements.

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“…Thus, sensory isolation may not be informative of the sensory dynamics under natural conditions, when a suite of senses participate. Instead, we present conflicting visual and mechanosensory stimuli to dissociate the two modalities while maintaining the sensory pathways intact-similar to human psychophysical experiments in reaching (1) and posture control (6) and experiments in joint visual-electrosensory tracking behaviors in knifefish (7).…”

mentioning

confidence: 99%

Integration of parallel mechanosensory and visual pathways resolved through sensory conflict

Roth

Hall

Daniel

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The acquisition of information from parallel sensory pathways is a hallmark of coordinated movement in animals. Insect flight, for example, relies on both mechanosensory and visual pathways. Our challenge is to disentangle the relative contribution of each modality to the control of behavior. Toward this end, we show an experimental and analytical framework leveraging sensory conflict, a means for independently exciting and modeling separate sensory pathways within a multisensory behavior. As a model, we examine the hovering flower-feeding behavior in the hawkmoth Manduca sexta. In the laboratory, moths feed from a robotically actuated two-part artificial flower that allows independent presentation of visual and mechanosensory cues. Freely flying moths track lateral flower motion stimuli in an assay spanning both coupled motion, in which visual and mechanosensory cues follow the same motion trajectory, and sensory conflict, in which the two sensory modalities encode different motion stimuli. Applying a frequency-domain system identification analysis, we find that the tracking behavior is, in fact, multisensory and arises from a linear summation of visual and mechanosensory pathways. The response dynamics are highly preserved across individuals, providing a model for predicting the response to novel multimodal stimuli. Surprisingly, we find that each pathway in and of itself is sufficient for driving tracking behavior. When multiple sensory pathways elicit strong behavioral responses, this parallel architecture furnishes robustness via redundancy.sensory integration | redundancy | animal locomotion | control theory | system identification A nimals rely on a convergence of information across parallel sensory pathways to control locomotion. In these neural control strategies, one sensory modality may contribute concurrently to several behaviors (a one-to-many mapping), and conversely, several sensory modalities may collectively govern a single behavior (a many-to-one mapping). A continuing aim in studies of animal behavior is to extricate the contribution of an individual sensory modality from the ensemble of pathways (that is, the one-to-one mapping from a sensory percept to the locomotor action; e.g., the optomotor response, chemotaxis, vestibular postural reflex, etc.). The dynamics of locomotor behaviors, however, are shaped by the combination of and interactions between sensorimotor pathways. Therein remains a fundamental challenge in understanding multisensory integration: how does the nervous system combine these streams of information to control behavior, and how do we separate the relative contributions of sensory pathways in the context of a parallel topology?There is no single answer. Across taxa and behaviors, nervous systems instantiate varied policies for integrating sensory information across modalities. In many instances, parallel sensory pathways serve complementary roles. For example, when humans perform reaching tasks, the planning of motion trajectories relies heavily on visual information, wher...

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Dynamic modulation of visual and electrosensory gains for locomotor control

Cited by 26 publications

References 41 publications

Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fish Gnathonemus petersii

Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fish Gnathonemus petersii

Multisensory Control of Orientation in Tethered Flying Drosophila

Integration of parallel mechanosensory and visual pathways resolved through sensory conflict

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