Odorant-induced oscillations in the mushroom bodies of the locust

By Gilles Laurent, Mohammad Naraghi. 1994

Kenyon cells are the intrinsic interneurons of the mushroom bodies in the insect brain, a center for olfactory and multimodal processing and associative learning. These neurons are small (3–8 microns soma diameter) and numerous (340,000 and 400,000 in the bee and cockroach brains, respectively). In Drosophila, Kenyon cells are the dominant site of expression of the dunce, DC0, and rutabaga gene products, enzymes in the cAMP cascade whose absence leads to specific defects in olfactory learning. In honeybees, the volume of the mushroom body neurophils may depend on the age or social status of the individual. Although the anatomy of these neurons has been known for nearly a century, their physiological properties and the principles of information processing in the circuits that they form are totally unknown. This article provides a first such characterization. The activity of Kenyon cells was recorded in vivo from locust brains with intracellular and local field potential electrodes during olfactory processing. Kenyon cells had a high input impedance (approximately 1 G omega at the soma). They produced action potentials upon depolarization, and consistently showed spike adaptation during long depolarizing current pulses. They generally displayed a low resting level of spike activity in the absence of sensory stimulation, despite a large background of spontaneous synaptic activity, and showed no intrinsic bursting behavior. Presentation of an airborne odor, but not air alone, to an antenna evoked spatially coherent field potential oscillations in the ipsilateral mushroom body, with a frequency of approximately 20 Hz. The frequency of these oscillations was independent of the nature of the odorant. Short bouts of oscillations sometimes occurred spontaneously, that is, in the absence of odorant stimulation. Autocorrelograms of the local field potentials in the absence of olfactory stimulation revealed small peaks at +/- 50 msec, suggesting an intrinsic tendency of the mushroom body networks to oscillate at 20 Hz. Such oscillatory behavior could not be seen from local field potential recordings in the antennal lobes, and may thus be generated in the mushroom body, or via feedback interactions with downstream neurons in the protocerebrum. During the odor-induced oscillations, the membrane potential of Kenyon cells oscillated around the resting level, under the influence of excitatory inputs phase- locked to the field activity. Each phasic wave of depolarization in a Kenyon cell could be amplified by intrinsic excitable properties of the dendritic membrane, and sometimes led to one action potential, whose timing was phase-locked to the population oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135.001”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…not stereotyped (Figure 1A) (Murthy et al., 2008; Caron et al., 2013); that is, individual flies show distinct wiring patterns between projection neurons and KCs. Sparse activity of the KCs represents the identity of odors (Laurent and Naraghi, 1994; Perez-Orive et al., 2002; Turner et al., 2008).”
Functional analysis of a higher olfactory center, the lateral horn (2012, background): “We identified additional GABAergic fibers of unknown origin running along the pedunculus to the accessory calyx (but not projecting to the LH); because KCs in the olfactory system do not project to the accessory calyx (Laurent and Naraghi, 1994), these fibers are unlikely to inhibit the KCs.”
GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system (1996, methodology): “Anatomical (Pearson, 1971; Schumann, 1974, 1987; Mobbs, 1982) and physiological (Menzel, 1987; Kanzaki et al., 1987; Erber et al., 1993; Laurent and Naraghi, 1994; Laurent and Davidowitz, 1994) evidence indicates that the calyx constitutes the main input site for sensory information from the…”
Speed and accuracy of olfactory discrimination in the rat (2003, background): “On a slow time scale, firing patterns evolve over hundreds of milliseconds to seconds during constant stimulus presentatio”
Conditional modulation of spike-timing-dependent plasticity for olfactory learning (2012, background): “In the context of reinforcer delivery, STDP gains a new role: it tags—presumably through biochemical changes dependent on pairing—the synapses between connected Kenyon cells and bLNs that have fired an action potential within the STDP pairing window, itself commensurate with the oscillation period i”
Olfactory representations by Drosophila mushroom body neurons. (2008, background): “These volleys occur periodically at a frequency of ϳ20 Hz, generating synchronized oscillations in the KC membrane potential (Laurent and Naraghi 1994; Perez-Orive et al. 2002).”
Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. (2003, background): “At higher fine the response of projection neurons to different odor concentrations that are likely to exceed those enodors (Imamura et al., 1992; Laurent and Naraghi, 1994; countered in natural environment, several glomeruli ap- Yokoi et al., 1995).”
Using noise signature to optimize spike-sorting and to assess neuronal classification quality. (2002, methodology): “All experiments were carried out on adult locusts (Schistocerca americana ) of both sexes, taken from a crowded colony and prepared as described in Laurent and Naraghi (1994).”
Encoding and decoding of overlapping odor sequences. (2006, unknown): “Neuron 476 The relevance of this time scale in locust is determined by the integrative properties of Kenyon cells, the PNs’ targets in the mushroom bodies (Laurent and Naraghi, 1994; Perez-Orive et al., 2002).”
Normalization for Sparse Encoding of Odors by a Wide-Field Interneuron (2011, background): “The baseline activity of KCs is close to 0 (7, 10, 13, 14), their responses to odors typically contain less than 3 action potentials, and the gain of their output synapses (the effectiveness of their rarely elicited spikes) is both high on average and modifiable by a Hebbian learning rule (15).”
Oscillatory integration windows in neurons (2016, methodology): “KC somata could be targeted unambiguously above the mushroom body calyx (Laurent and Naraghi, 1994).”
A Simple Connectivity Scheme for Sparse Coding in an Olfactory System (2007, methodology): “…vector and (2) so that these KCs will safely pass firing threshold, exploiting both a small surplus of excitation from a smaller set of less reliable PNs in that integration cycle (Mazor and Laurent, 2005), and nonlinear summation (Laurent and Naraghi, 1994; Perez-Orive et al., 2002, 2004).”
Imaging a Population Code for Odor Identity in the Drosophila Mushroom Body (2013, background): “The odor responses of Kenyon cells (KCs), the principle neurons of the MB, are substantially more selective than their antennal lobe inputs (Laurent and Naraghi, 1994; Perez-Orive et al., 2002; Turner et al., 2008; Wang et al., 2008; Honegger et al., 2011).”
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition (2010, background): “Synchronous fast oscillations are prominent in the olfactory system and play a major role in odor stimulus processing (79, 117, 161, 303, 308, 441, 461, 501, 503, 555, 556, 584, 847, 1043).”