Mechanisms and Function of Neural Synchronization in an Insect Olfactory System

Citation

MacLeod, Katrina Marie (1999) Mechanisms and Function of Neural Synchronization in an Insect Olfactory System. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/GYVD-3755. https://resolver.caltech.edu/CaltechTHESIS:04202017-091931686

Abstract

One of the fundamental questions in modem integrative neurobiology relates to the encoding of sensory information by populations of neurons, and to the significance of this activity for perception, learning, memory and behavior. Synchronization of activity across a population of neurons has been observed many times over, but has never been demonstrated to be a necessary component of this coding process. Neural synchronization has been found in many brain areas in animals across several phyla, from molluscs to mammals. Studies in mammals have correlated the degree of neural synchronization with specific behavioral or cognitive states, such as sensorimotor tasks, segmentation and binocular rivalry suggesting a functional link. In the locust olfactory system, oscillatory synchronization is a prominent feature of the odor-evoked neural activity. Stimulation of the antenna by odors evokes synchronized firing in dynamic and odor-specific ensembles of the projection neurons of the antennal lobe, the principal neurons of the first-order olfactory relay in insects. The coherent activity of these projection neurons underlies an odor-evoked oscillatory field potential which can be recorded in the mushroom body, the second-order olfactory relay to which they project.

In this dissertation, we investigated two important questions raised by these findings: how are such stimulus-evoked synchronous ensembles generated, and what is their functional significance? To address these questions, we performed electrophysiological experiments and recorded odor responses from neurons of the antennal lobes and mushroom bodies of locusts, in vivo and using natural odor stimulation in an unanesthetized, semi-intact preparation.

We demonstrated the critical mechanism involved in neural synchronization of the antennal lobe neurons. The synchronization of the projection neurons relies critically on fast GABA (γ-aminobutyric acid) -mediated inhibition from the local interneurons. Projection neuron synchronization could be selectively blocked by local injection of the GABA receptor antagonist, picrotoxin. Picrotoxin spared the odor-specific, slow modulation of individual projection neuron responses, but desynchronized the firing of the odor-activated projection neuron assemblies. The oscillatory activity of the local intemeurons was also blocked by picrotoxin, which indicates that such activity depends on network synaptic dynamics. We also showed that the mushroom body networks are capable of generating oscillatory behavior of a similar frequency as that of its projection neuron inputs, and that they may thus be "tuned" to accept synchronized, oscillatory inputs of that frequency range.

Our understanding of this mechanism, in tum, made possible the functional investigation of neural synchronization by selective disruption of projection neuron synchronization. We studied a population of neurons downstream from the antennal lobe projection neurons, the extrinsic neurons of the β-lobe of the mushroom body (βLNs). These βLNs were chosen for investigation because they were found to be odor-responsive and because their position in the olfactory pathway makes them a suitable "read-out" of population activity in the antennal lobe. We characterized βLN odor responses before and after selective disruption of the synchronization of the projection neuron ensembles with local picrotoxin injection into the antennal lobe. We showed that the tuning of these βLN responses was altered by PN desynchronization by changing existing responses and inducing new responses. This alteration in tuning resulted in a significant loss of odor specificity in individual βLN responses, an effect that never occurred in the responses of individual, desynchronized projection neurons. We thus propose that neural synchronization is indeed important for information processing in the brain: it serves, at least in part, as a temporal substrate for the transmission of information that is contained across co-activated neurons (relational code) early in the pathway.

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