How do neural circuits control behavior? How has oriented behavior evolved? How can neural circuits evolve to meet the ecological needs of different species, living in different environments, pursuing different behavioral strategies?
These are some of the questions asked in our group. To answer them, we employ a wide range of methods, from volume electron microscopy and comparative connectomics, classic neuroanatomy, functional studies using electrophysiology, all the way to behavioral experiments. To link circuit anatomy to functional data, we generate biologically constrained computational models of neural circuits, producing testable hypotheses that are directly pursued using functional and behavioral experiments.
Our model system is the central complex in the insect brain. This brain region lies at the core of the insect brain and is responsible for selecting behaviors that are appropriate for any given moment in time. It combines sensory signals with context cues to generate motor commands and thus integrates the current state of the world with previous experience and internal state to guide the behavioral choices of the animal. In the context of orientation and navigation, this process can be studied in great detail, which is why our group focuses on this process. Here, the central complex computes the current heading of the animal (internal compass), computes an internal representation of its current goal direction (desired heading), and compares the two angles to decide whether to turn right or left (steering control).
Fundamental to this process is the intricate neural circuitry of this brain region and the unusually tight structure function relations that define the computations carried out by the central complex. These computational essentially boil down to comparing the phase and amplitude of sinusoidal patterns of neural activity. These patterns emerge from populations of identical neurons distributed across the anatomical width of the central complex. These patterns represent vectors with the peak of the activity bump being the direction of the vector in 2D space and the amplitude, possibly, representing the vector length. By shifting these patterns relatively to each other, and adding and subtracting them from one another, the anatomical backbone of the central complex neural circuitry, likely performs all computations needed to generate context dependent oriented behavior.
The intricate, sophisticated neural arrangement of the central complex did not emerge out of nowhere, but has evolved over at least 450 millions years, since the dawn of the insects. We find over 1 million species of insects on the planet, inhabiting all imaginable habitats, pursuing a wide range of behavioral strategies. Yet the central complex, supposedly controlling behavior in all these species, appears to be extremely conserved. How can a single brain region control all these different behaviors? How can such a fundamentally important circuit even change without being disrupted in the process? To answer these questions we have embarked on a mission to delineate the neural circuits of the central complex across the insect phylogenetic tree - at the level of synapses. We are constructing connectomes of the central complex from up to 20 insect species, aiming at identifying the conserved ground pattern and the diverse solutions these species have found to similar and specific ecological problems. This will hopefully lead us towards understanding the origin of oriented behavior, lead us to uncover principles of how complex neural circuits can evolve, and how the neural computations of the brain are translated into distinct, species specific behaviors.