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.

How should biological behaviour be modelled? A relatively new approach is to investigate problems in neuroethology by building physical robot models of biological sensorimotor systems. The explication and justification of this approach are here placed within a framework for describing and comparing models in the behavioural and biological sciences. First, simulation models – the representation of a hypothesis about a target system – are distinguished from several other relationships also termed “modelling” in discussions of scientific explanation. Seven dimensions on which simulation models can differ are defined and distinctions between them discussed:1. Relevance: whether the model tests and generates hypotheses applicable to biology.2. Level: the elemental units of the model in the hierarchy from atoms to societies.3. Generality: the range of biological systems the model can represent.4. Abstraction: the complexity, relative to the target, or amount of detail included in the model.5. Structural accuracy: how well the model represents the actual mechanisms underlying the behaviour.6. Performance match: to what extent the model behaviour matches the target behaviour.7. Medium: the physical basis by which the model is implemented.No specific position in the space of models thus defined is the only correct one, but a good modelling methodology should be explicit about its position and the justification for that position. It is argued that in building robot models biological relevance is more effective than loose biological inspiration; multiple levels can be integrated; that generality cannot be assumed but might emerge from studying specific instances; abstraction is better done by simplification than idealisation; accuracy can be approached through iterations of complete systems; that the model should be able to match and predict target behaviour; and that a physical medium can have significant advantages. These arguments reflect the view that biological behaviour needs to be studied and modelled in context, that is, in terms of the real problems faced by real animals in real environments.

Ants, like many other animals, use visual memory to follow extended routes through complex environments, but it is unknown how their small brains implement this capability. The mushroom body neuropils have been identified as a crucial memory circuit in the insect brain, but their function has mostly been explored for simple olfactory association tasks. We show that a spiking neural model of this circuit originally developed to describe fruitfly (Drosophila melanogaster) olfactory association, can also account for the ability of desert ants (Cataglyphis velox) to rapidly learn visual routes through complex natural environments. We further demonstrate that abstracting the key computational principles of this circuit, which include one-shot learning of sparse codes, enables the theoretical storage capacity of the ant mushroom body to be estimated at hundreds of independent images.

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