Abstract

Contrary to popular notions, insects have sophisticated brains that allow them to adjust control so that behaviors are consistent with current internal and external conditions. The Central Complex (CX) is a set of midline neuropils in the brains of all arthropods. It is made up of the columnar structures including the protocerebral bridge, fan-shaped body and ellipsoid body. Neurons in these structures project to the paired nodules and lateral accessory lobes where they have access to descending interneurons that alter movements.

Over the past couple of decades, the CX has received a remarkable amount of attention by insect neurobiologists. We now know that several types of sensory information projects to the CX including mechanical information from the antennae and various visual cues including polarized light. Polarized light is used by several migratory insects to guide their long distance flights. We also know that activity in the CX precedes changes in movement and stimulation in the same regions can evoke turning behavior. Recently, navigation cues such as head direction compass cells have been identified in several insects.

Cockroaches are scavengers that forage through darkened environments. Like many foraging insects, they must keep track of targets while negotiating barriers. Thus, they need to simultaneously integrate sensory information and produce appropriate motor commands. As cockroaches move toward a darkened shelter they continually asses their situation and decide to either continue or turn based on whether they still see the shelter (Daltorio et al., 2013). This foraging behavior requires that the insect know its orientation and the direction of recent turns. It must then use that information to influence descending commands that result in turning behaviors. By performing tetrode recordings in a restrained preparation, we found CX neurons that encode the animal’s orientation using external and internal sensory cues, similarly to mammalian head direction cells as well as the direction of recent rotations (Varga and Ritzmann, 2016). How can this information influence movement in the arena? We recorded from tethered and freely walking cockroaches and found CX neurons in which activity increased just prior to changes in direction or speed (Martin et al., 2015). The patterns of movement coded in each CX neuron represents a population code that covers the entire range of horizontal movements that cockroaches make in the arena. Moreover, stimulation through the same tetrodes evoked movements consistent with the recorded activity. For individuals that consistently evoked turning in a particular direction, we further examined leg reflexes associated with the femoral chordotonal organ (FCo), which evokes reflex changes in the motor neurons that control the femur-tibia joint as well as the adjacent coxa-trochanter joint. Lesion of all descending activity causes a reversal in the FCo reflex to the slow depressor neuron (Ds) of the coxa-trochanter joint, which is consistent with changes associated with turning. Together these studies demonstrated that the cockroach CX relies upon a variety of sensory modalities to encode the animal’s orientation, which is then used to generate directionally specific motor commands, and therefore, direct locomotion.

More recently, we have turned to an insect predator to expand our understanding of how brain systems alter behavior. Predators must track down and accurately strike prey. Many change their strategy for obtaining food as they become satiated. We have been able to tap into CX activity during this process and have begun to examine how neuromodulators associated with satiety alter CX activity and related stalking behavior.

Bio

Roy E. Ritzmann is a Professor in the Department of Biology at Case Western Reserve University in Cleveland, Ohio. He received the B.A. degree in Zoology from the University of Iowa, the Ph.D. in Biology from the University of Virginia then moved to a postdoctoral position at Cornell University where he began working with insects on the neural circuitry underlying escape systems. His laboratory focuses on behavioral and neural properties that are involved in insect movement around barriers in complex terrain most recently focusing upon context and state dependent control in an insect brain region called the central complex (a group of neuropils that reside on the midline of virtually all arthropod brains). To that end they employ both extracellular (multi-channel) and intracellular recording techniques in the brain and thoracic ganglia of cockroaches and praying mantises. Using these techniques the Ritzmann laboratory has made progress in understanding how the central complex integrates massive amounts of information on the insect’s surroundings and internal state into descending commands that adjust movements toward goals and away from threats in a context dependent fashion. The Ritzmann laboratory has also collaborated on many biologically inspired robotic projects.