Integration of parallel mechanosensory and visual pathways resolved through sensory conflict

Abstract

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...

Dynamic modulation of visual and electrosensory gains for locomotor control

“…Control theory provides a common framework to quantify and interpret the behaviour of the whole animal through perturbations to exogenous reference signals and measurements of corresponding behavioural responses (for reviews, see [13,14]). Closed-loop neuromechanical modelling has been used to investigate the feedback control of diverse biological systems and behaviours, including flight control in moths [15,16] and flies [17 -19], flower tracking in moths [20], postural balance in humans [21,22] and refuge-tracking in fish [8,23,24].…”

Responses to mechanically and visually cued water waves in the nervous system of the medicinal leech

“…A notable vertebrate example is the mottled sculpin Cottus bairdi, of which lake and river populations weigh the two modalities differentially (Coombs and Grossman, 2006). Likewise, the hawkmoth Manduca sexta relies on the integration of these same two modalities to stabilize its flight (Roth et al, 2016). The leech, with its comparatively much smaller nervous system, cannot match these other animals in sophistication of behavior, but it presents a rare opportunity to study sensory integration in a simple and accessible nervous system.…”

Insect and insect-inspired aerodynamics: unsteadiness, structural mechanics and flight control

“…In any case, it is clear that flight control is typically multimodal with mechanosensation working in tandem with vision and various methods are available that can disentangle the cues (e.g. [75,76]). A comprehensive recent study [77] has shown that generation of steering motor commands that are known to be the result of visual perception, is modulated (in opposing ways) by mechanosensory information from the wings and halteres.…”