Robots with insect brains

Summary Many animals navigate using a combination of visual landmarks and path integration. In mammalian brains, head direction cells integrate these two streams of information by representing an animal's heading relative to landmarks, yet maintaining their directional tuning in darkness based on self-motion cues. Here we use two-photon calcium imaging in head-fixed flies walking on a ball in a virtual reality arena to demonstrate that landmark-based orientation and angular path integration are combined in the population responses of neurons whose dendrites tile the ellipsoid body — a toroidal structure in the center of the fly brain. The population encodes the fly's azimuth relative to its environment, tracking visual landmarks when available and relying on self-motion cues in darkness. When both visual and self-motion cues are absent, a representation of the animal's orientation is maintained in this network through persistent activity — a potential substrate for short-term memory. Several features of the population dynamics of these neurons and their circular anatomical arrangement are suggestive of ring attractors — network structures proposed to support the function of navigational brain circuits.

Path integration is a widespread navigational strategy in which directional changes and distance covered are continuously integrated on an outward journey, enabling a straight-line return to home. Bees use vision for this task – a celestial-cue based visual compass, and an optic-flow based visual odometer – but the underlying neural integration mechanisms are unknown. Using intracellular electrophysiology, we show that polarized-light based compass-neurons and optic-flow-based speed-encoding neurons converge in the central complex of the bee brain, and through block-face electron microscopy we identify potential integrator cells. Based on plausible output targets for these cells, we propose a complete circuit for path integration and steering in the central complex, with anatomically-identified neurons suggested for each processing step. The resulting model-circuit is thus fully constrained biologically and provides a functional interpretation for many previously unexplained architectural features of the central complex. Moreover, we show that the receptive fields of the newly discovered speed neurons can support path integration for the holonomic motion (i.e. a ground velocity that is not precisely aligned with body orientation) typical of bee-flight, a feature not captured in any previously proposed model of path integration. In a broader context, the model-circuit presented provides a general mechanism for producing steering signals by comparing current and desired headings – suggesting a more basic function for central-complex connectivity from which path integration may have evolved.

Many animals rely on a sun compass for spatial orientation and long-range navigation. In addition to the Sun, insects also exploit the polarization pattern and chromatic gradient of the sky for estimating navigational directions. Analysis of polarization-vision pathways in locusts and crickets has shed first light on brain areas involved in sky compass orientation. Detection of sky polarization relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Brain areas involved in polarization processing include parts of the lamina, medulla and lobula of the optic lobe and, in the central brain, the anterior optic tubercle, the lateral accessory lobe and the central complex. In the optic lobe, polarization sensitivity and contrast are enhanced through convergence and opponency. In the anterior optic tubercle, polarized-light signals are integrated with information on the chromatic contrast of the sky. Tubercle neurons combine responses to the UV/green contrast and e-vector orientation of the sky and compensate for diurnal changes of the celestial polarization pattern associated with changes in solar elevation. In the central complex, a topographic representation of e-vector tunings underlies the columnar organization and suggests that this brain area serves as an internal compass coding for spatial directions.