The Neural Basis Of Head Direction And Spatial Context In The Insect Central Complex

The Neural Basis of Head Direction and Spatial Context in the Insect Central Complex

A question of wide importance in neuroscience is how the brain controls behavior. How does sensory information get transformed into a spatially organized representation about our current state in the world and how is this abstract representation utilized when producing motor commands that lead to successful navigation? When navigating in a complex environment, all animals must encode information about their position and orientation in a rich sensory environment. In vertebrates this may occur by means of distributed activity across several navigation circuits located in the hippocampal formation. Arthropods, however, lack a hippocampal formation and thus it is unclear what circuits mediate navigation. A wide range of studies indicate that the central complex (CX), is not only involved in directional sensory information processing and the control of motor commands, but also plays a role in orientation coding in polarized light guided navigation and landmark orientation. All of these neural mechanisms point in the direction that single neurons in the CX might be directly involved in head direction coding, as well as other aspects of adaptive navigation. In the work described in this dissertation I used multi-channel extracellular recording techniques to uncover the neural correlates of head direction coding and spatial context cues in the cockroach CX. Specifically, I used tetrodes to record the activity of single neurons in the CX while the animal was passively rotated around on a platform surrounded by a circular arena (Chapter 2). In the same setting I also recorded local field potentials (LPFs) in the CX to uncover how navigational information modulates the network’s activity in a more global manner (Chapter 3). I found that single units, as well as LFPs in the cockroach CX encode the animal’s head direction relative to a salient visual cue. However, when landmarks are not available to the animal, both single neuron and network-level activity can rely upon idiothetic motion cues to update the animal’s relative heading in a landmark-free setting. In addition to these results, I found that a subpopulation of single neurons and some of the LFP frequency bands encoded the rotation direction history of the animal, a common spatial context cue. These results suggest that the CX navigation circuit is involved in environmental context discrimination processes that might be utilized by spatial memory circuits in the insect brain.Taken together, these results provide a solid foundation for future studies on the neural basis of adaptive navigation in insects. By placing these results in a wider context of adaptive navigation in all animals and by comparing them to the mechanisms described in mammalian navigation circuits, these data also contribute to a broad comparative approach to understand the general principles of navigation, as well as the diversity of the neural substrates of navigation across evolutionarily distinct animals.

The Insect Central Complex – From Sensory Coding to Directing Movement

The Oxford Handbook of Invertebrate Neurobiology

Invertebrates have proven to be extremely useful model systems for gaining insights into the neural and molecular mechanisms of sensory processing, motor control and higher functions such as feeding behavior, learning and memory, navigation, and social behavior. A major factor in their enormous contributions to neuroscience is the relative simplicity of invertebrate nervous systems. In addition, some invertebrates, primarily the molluscs, have large cells, which allow analyses to take place at the level of individually identified neurons. Individual neurons can be surgically removed and assayed for expression of membrane channels, levels of second messengers, protein phosphorylation, and RNA and protein synthesis. Moreover, peptides and nucleotides can be injected into individual neurons. Other invertebrate model systems such as Drosophila and Caenorhabditis elegans offer tremendous advantages for obtaining insights into the neuronal bases of behavior through the application of genetic approaches. The Oxford Handbook of Invertebrate Neurobiology reviews the many neurobiological principles that have emerged from invertebrate analyses, such as motor pattern generation, mechanisms of synaptic transmission, and learning and memory. It also covers general features of the neurobiology of invertebrate circadian rhythms, development, and regeneration and reproduction. Some neurobiological phenomena are species-specific and diverse, especially in the domain of the neuronal control of locomotion and camouflage. Thus, separate chapters are provided on the control of swimming in annelids, crustaea and molluscs, locomotion in hexapods, and camouflage in cephalopods. Unique features of the handbook include chapters that review social behavior and intentionality in invertebrates. A chapter is devoted to summarizing past contributions of invertebrates to the understanding of nervous systems and identifying areas for future studies that will continue to advance that understanding.