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Olfactory Processing: Massive result in the sparse and highly selective responses Convergence onto Sparse Codes observed in Kenyon cells? Jortner et al. [6] note that three mechanisms sharply constrain the Sparse provides numerous computational advantages. A ability of Kenyon cells to spike recent analysis of the locust olfactory system has revealed a surprising unless odor-driven conditions are circuit solution for achieving remarkably sparse and specific neural met. First, projection neurons representations of odors. respond to odors with temporally complex firing patterns that include Mark Stopfer fundamental circuit properties of periods of inhibition, so, of all connectivity and response projection neurons converging Sparse coding, a neural threshold. upon a Kenyon cell, only an information processing strategy How to characterize the odor-specific subset is active at featuring minimal, broadly connectivity matrix linking 830 any given time. Second, individual distributed spiking activity, projection neurons to 50,000 EPSPs triggered by projection appears to be common across Kenyon cells? Jortner et al. [6] first spikes are very tiny — two brain areas and species. How is considered the branching patterns orders of magnitude smaller than sparse coding achieved by neural of these neurons. In confocal the firing threshold of Kenyon circuitry? In the locust olfactory images of the locust brain they cells — so many projection system, olfactory receptor noted very extensive spatial neurons need to fire together neurons project to the antennal overlaps between dye-filled to trigger a Kenyon cell spike. lobe (analogous to the vertebrate projection neuron and And third, shutter-like, rhythmic olfactory bulb), where they Kenyon cell such that feed-forward inhibition onto the upon a population of large numbers of projection Kenyon cells, driven indirectly by excitatory projection and inhibitory neurons appeared to contact each the oscillatory output of projection local neurons. Odor-driven circuit Kenyon cell. But were these neurons, prohibits Kenyon cells interactions coordinate these apparent contacts functional? The from firing during a portion of each neurons into widespread authors devised an elegant oscillatory cycle; projection oscillatory synchrony [1], and physiology experiment: they neurons rarely fire more than once transform representations of any systematically made extracellular per cycle. These conditions ensure given odor into specific, reliable, ‘tetrode’ recordings from Kenyon cells spike rarely and exuberant and temporally groups of projection neurons to specifically; Jortner et al.’s [6] complex patterns of action monitor their spontaneous analysis of these conditions is potentials [2,3] distributed across spiking while making an quantitative, and the numbers the majority of the 830 or so intracellular recording from work out. projection neurons (analogous to a Kenyon cell to monitor its Massively convergent wiring the vertebrate mitral cells). excitatory post-synaptic seems an odd way to construct Projection neurons, in turn, potentials (EPSPs). Although a sparse representation. Yet, synapse upon a group of about these individual EPSPs were tiny, Jortner et al. [6] used the simple 50,000 follower neurons, the typically buried in the noise that is binomial coefficient equation Kenyon cells, within the mushroom characteristic of such recordings, to demonstrate that this body (Figure 1), a structure the authors revealed them by arrangement is, in fact, optimal: analogous to the vertebrate averaging many traces that had 50% connectivity maximizes the piriform cortex. Interestingly, been aligned with respect to unique projection neuron Kenyon cells are nearly silent. They spikes in projection neurons. A combinations Kenyon cells could respond to odors rarely and barely, convincing series of control sample. The resulting number of often with just a spike or two, but measures indicated that these potential combinations vastly reliably and with remarkable EPSPs were most likely exceeds the actual number of specificity [4]. In the course of an elicited monosynaptically Kenyon cells; thus, there is experiment, a given Kenyon cell is by the spikes in the projection essentially no chance that any two likely to fire not at all, or only when neurons. Kenyon cells will sample the the animal’s antenna encounters This analysis showed, same group of projection neurons. a particular odorant, or even remarkably, that each Kenyon cell This dense connectivity matrix, a particular concentration of an received direct input from about therefore, optimizes the odorant [5]. Thus, there is sparse half of the projection neurons differences between inputs, coding: for a given stimulus, very tested — extrapolating from the leading to well-separated, sparse few of the huge population of dataset suggested every Kenyon representations of odors. Odor Kenyon cells respond at all, and the cell sampled the output of about representations in Kenyon cells response consists of very few 415 of the 830 projection neurons. have less overlap with each spikes. A recent paper by Jortner This seems paradoxical: how can other than representations in et al. [6] examined how this sparse such massively convergent input projection neurons, with coding arises from the from so many rapid-fire projection attendant advantages for Current Biology Vol 17 No 10 R364

coding. As these recent publications show, it will be KCs: 50,000 essential and interesting to understand the anatomical and physiological features that make sparse codes possible.

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[10,11] and appear to make the locust. many fewer synaptic contacts Although it’s too soon to NIH-NICHD, 35 Lincoln Drive, [12]. Thus, in Drosophila, sparse generalize about the prevalence Rm 3A-102, msc 3715, Bethesda, coding may be achieved by and utility of different Maryland 20892, USA. a mechanism somewhat underlying mechanisms, it E-mail: [email protected] different from that of appears there is more than the locust. one way to achieve sparse DOI: 10.1016/j.cub.2007.03.019