I am grateful to all members of the Laurent laboratory, past and present, who offered thoughtful critiques and incredible support. In the locust olfactory system, oscillatory synchronization is a prominent feature of the odor-evoked neural activity. Stimulation of the antenna by odors elicits synchronized firing in dynamic and odor-specific ensembles of antennal projection neurons.
The synchronization of the projection neurons is critically dependent on fast GABA (γ-aminobutyric acid)-mediated inhibition by the local intemeurons. The synchronization of projection neurons 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.
We studied a population of neurons downstream of the antenna! lobe projection neurons, the extrinsic neurons of the P-lobe of the mushroom body CPLNs). We characterized PLN odor responses before and after selective disruption of the synchronization of the projection neuron ensembles with local picrotoxin injection into the antenna.
Background and significance
Introduction
We discuss here the structure (section III) and function (section IV) of the olfactory systems of insects and vertebrates, including several explicit models of olfactory function. For space reasons, the discussion is limited to these two systems, although the olfactory systems of crustaceans, molluscs, and other invertebrates could also be involved. Also in Section IV we discuss the specific finding of oscillatory neural synchronization, another common feature, in the olfactory systems of locusts and vertebrates.
Synchronization has also been described in the visual, auditory and somatomotor cortical and subcortical areas and in the hippocampus. We review a selection of these results, and the proposed mechanisms to underlie synchronization in these systems (Section V).
Olfactory Coding
Animals may need to detect hundreds or thousands of odor molecules present in the environment. Detection of molecules occurs with olfactory receptor neurons that are positioned to be accessible by air or water odors in the environment. In generalist olfaction, most neural responses in the periphery and central nervous system are broadly tuned.
These findings indicate that information about odor identity is contained in the identity of neurons activated by a stimulus. Of central importance to this thesis, oscillatory neural synchronization is a widespread phenomenon in olfactory systems in several phyla, from molluscs to mammals. First, a 4–12 Hz rhythm, designated the theta rhythm, is found in the olfactory bulb and olfactory cortex of vertebrates and appears to be related to the frequency of sniffing, at least in small mammals (Buonviso et al., 1992; Chaput and Holley, 1980; Chaput, 1986; Sobel and Tank, 1993).
Work in the hippocampus suggests that the theta rhythm may be involved in memory processes or spatial encoding (Burgess et al., 1994; O'Keefe and Reece, 1993). In the olfactory system of locusts, we proposed the hypothesis that the identity of odorants is encoded by a distributed and dynamic code of oscillatory sequences of synchronized neural circuits (Laurent and Davidowitz, . 1994; Laurent et al., 1996; Laurent, 1996).
The Olfactory System
The basal dendrites of the mitral cells contact a population of local intemeurons in the external plexiform layer, the granule cells. The olfactory bulb thus uses the neurotransmitters typical of the vertebrate brain: glutamate (and possibly aspartate) and GABA. However, a minority of the antennal nerve axons project to the posterior part of the nerve.
In locusts, the axons of the PNs assemble into a single dense bundle ( Leitch and Laurent, 1996 ), which forms the antennoglomerular tract (AGT). The main axon of each PN continues to terminate in the lateral lobe of the protocerebrum. In the grasshopper, the axonless local interneurons (LNs) of the AL differ from the projection neurons in their morphology and physiology.
Several differences exist in the anatomy and structure of the AL of locust versus other well-studied species. It is located in much of the protocerebrum, including the calyxes of the mushroom body, the antenna. lobes and the lateral lobes.
Physiology of the olfactory system
One obvious feature of activity patterning in the responses of olfactory bulb neurons is the respiratory rhythm (Chaput and Holley, 1980; Chaput, 1986). There have been relatively few studies of the piriform cortex compared to the olfactory bulb, possibly due to its relative inaccessibility. Berger's invention of electroencephalographic recording (EEG) in the late 1920s led to the discovery of brain waves: oscillatory potentials are so widespread and coherent that they can be recorded from the scalp, establishing the generation of oscillatory activity in the brain (Berger, 1929) .
Blocking inhibitory mechanisms in the olfactory bulb appears to alter the firing rate and tuning of odor responses in principal neurons (Yokoi et al., 1995). One pattern is simply that of the external stimulus (the combination of odor molecules and/or their steric/chernic properties, or 'odotopes' (Shepherd, 1991)). An explicit model of the insect macroglomerular complex was investigated using a small network of neurons (Linster et al., 1993).
A large-scale model of the piriform cortex (Wilson and Bower, 1992) constrained by physiological and anatomical considerations successfully reproduced one of the well-known features of olfactory cortex: the oscillatory activity due to electrical and olfactory stimuli (Freeman, 1968b; Bressler and Freeman, 1980). In summary, the results of these modeling studies suggest that the temporal patterning of odor responses in the olfactory bulb and antenna.
Synchronization in other systems
Efferent projections of the primary and accessory olfactory bulb in the tree shrew (Tupaia glis).
Origin and mechanisms of synchronization of antenna! lobe neurons
The effects of projection neuron desynchronization on the odor
Anatomical and physiological properties of mushroom body feedback neurons in the honey bee brain. Axonal projection patterns of mitral and tufted cells of the rat olfactory bulb. Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta.
Topographic organization of accessory fibers of the rat olfactory system, including centrifugal fibers in the olfactory bulb.
