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Olfactory Coding: Tagging and Tuning Odor-Activated Synapses for Memory

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Olfactory Coding: Tagging and Tuning Odor-Activated Synapses for Memory View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R227 11. Uhl, M.A., Biery, M., Craig, N., and 14. Keniry, M.E., Kemp, H.A., Rivers, D.M., and by systematic analysis of protein complexes. Johnson, A.D. (2003). Haploinsufficiency-based Sprague, G.F., Jr. (2004). The identification of Nature 415, 141–147. large-scale forward genetic analysis of Pcl1-interacting proteins that genetically 18. Huang, D., Friesen, H., and Andrews, B. (2007). filamentous growth in the diploid human interact with Cla4 may indicate a link between Pho85, a multifunctional cyclin-dependent fungal pathogen C.albicans. EMBO J. 22, G1 progression and mitotic exit. Genetics 166, protein kinase in budding yeast. Mol. Microbiol. 2668–2678. 1177–1186. 66, 303–314. 12. Bruno, V.M., Kalachikov, S., Subaran, R., 15. Cullen, P.J., and Sprague, G.F., Jr. (2012). 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Cell 19, Michon, A.M., Cruciat, C.M., et al. (2002). 2741–2751. Functional organization of the yeast proteome DOI: 10.1016/j.cub.2012.02.037 Olfactory Coding: Tagging and Tuning groups of projection neurons. These firing patterns are also segmented into Odor-Activated Synapses for Memory a sequence of time bins by w20 Hz oscillations generated in the antennal lobe [8–11]. Intensely spiking A recent study in the locust olfactory system shows how neuromodulators can projection neurons carry this alter the rules of synaptic plasticity to form associative memories through the information from the antennal lobe to use of ‘tagged’ synapses. the calyx of the mushroom body, where huge numbers of Kenyon cells respond Zane N. Aldworth and Mark Stopfer believed to help encode odors to the odor sparsely with spikes that and form memories. But the are few and far between [12,13]. Scents evoke vivid recollections — the odor-evoked spiking was ephemeral; Kenyon cells are influenced by the smell of sunscreen brings the ocean it ended several seconds before oscillatory patterning generated in to mind; a whiff of perfume calls forth a rewarding drop of sugar water the antennal lobe [9] and transmit a long-ago friend. It seems effortless was presented to the animal, long the oscillations to postsynaptic to form and remember powerful after the millisecond-scale time targets, including the mushroom connections between odors and other window for STDP had closed [4]. body’s b-lobes [14]. sensory stimuli. Yet, a physiological Behavioral tests showed this training Cassenaer and Laurent [3] had understanding of how our brains procedure induced new memories, previously shown that STDP can occur instantiate these associations remains but because pre- and post-synaptic at the synapse between Kenyon cells elusive. Hebb famously suggested [1] spiking linking odor and reward and b-lobe neurons in the locust. This that a synapse could be strengthened could not occur in these cells with first demonstration of STDP in an when the presynaptic and postsynaptic the required timing, STDP alone invertebrate showed that STDP acts neurons are activated together. The could not be responsible for forming here as a homeostatic mechanism, discovery of spike-timing-dependent them. How to resolve this dilemma? maintaining the integrity of the plasticity (STDP) [2], a process that An elegant new study by Cassenaer oscillatory signal passed along from can either increase synaptic strength and Laurent [5] points to a solution: the antennal lobe, rather than as (when the presynaptic cell is activated STDP can ‘tag’ an odor-activated a mechanism of memory. But in their milliseconds before the postsynaptic synapse, signifying and sustaining new work, Cassenaer and Laurent [5] cell), or decrease synaptic strength its identity until the reinforcement returned to the Kenyon cell–b-lobe (when the timing is reversed), provided signal arrives. neuron synapse to explore whether a physiological mechanism for this Because the insect olfactory system STDP there can be mnemonic. The plasticity. STDP has been shown to is relatively simple and accessible it authors first characterized responses occur in many species, including the has become a useful model for the of b-lobe neurons to a range of locust [3]. study of sensory processing and odorants believed relevant to behaving Connecting Hebbian STDP to the associative memory [6]. Odors are locusts. Consistent with previous formation of memory, however, has transduced by odorant receptors and studies [3,14], the authors found that been surprisingly difficult, partly their associated olfactory receptor the temporally patterned spiking because STDP operates at much neurons in the antennae (Figure 1A) responses of b-lobe neurons varied shorter time scales than the behavioral [7]. These afferent neurons carry with the odor, and that firing rates of the experiences that lead to new information to the antennal lobe, where b-lobe neuron vastly exceeded those memories. For example, a recent study lateral interactions among the receptor of their presynaptic Kenyon cells. showed that in moths, animals that neurons, local neurons and projection The authors also found individual readily learn to associate odors with neurons rearrange odor-evoked b-lobe neurons responded much less a tasty reward, odors reliably evoke responses into temporally structured selectively to odorants than did spiking in Kenyon cells, neurons long patterns of spiking distributed across individual Kenyon cells, and that their Current Biology Vol 22 No 7 R228 A S1 S2 BCcells was activated at delays much dt>0 dt<0 Response to Odor 1 longer than the STDP window bLN bLN At first KCs S1 S1 After Odor 2 + OCT S2 (stimulation at site S2 in Figure 1A,B) MB Calyx S2 After Odor 1 + OCT STDP STDP did not affect synaptic strength. bLN bLN S1 S1 S2 S2 These results revealed a new STDP + OCT STDP + OCT property of STDP: even though Antenna bLN bLN + S1 S1 + S2 S2 octopamine had spread throughout bLNs Test Test the b-lobe, its neuromodulatory ORNs S1 S2 S1 S2 MB β Lobe + effect occurred only at synapses -/+ bLN Response Rate PN that had been ‘tagged’ earlier by STDP. Avg EPSP Time Time Cassenaer and Laurent [5] found the + LN Before STDP STDP–octopamine modulation could Test EPSP After STDP take place when the b-lobe neurons Antennal Lobe After STDP + OCT Time Current Biology were activated by odorants rather than by current injection: odor-evoked b Figure 1. Neuromodulation of STDP in the insect olfactory system. firing rates of -lobe neurons dropped significantly after that odor (A) The locust olfactory system receives sensory input from olfactory receptor neurons (ORNs) mainly on the antennae. These neurons synapse with both local neurons (LNs) and projection had been paired with octopamine neurons (PNs) in the antennal lobe (AL), the first olfactory center within the brain. The PNs alone injection (Figure 1C). This reduction carry olfactory information to other areas of the brain, including the Kenyon cells (KCs) of the reflected a specific decrease in mushroom body calyx (MB calyx), which in turn synapse on the b-lobe neurons (bLNs). (B) synaptic strength that the modulator Spike-timing-dependent plasticity (STDP) was elicited at the KC–bLN synapse. Two well-sepa- induced between STDP-tagged rated groups of KCs in the mushroom body (MB; S1 and S2, one for pairing, one for control) presynaptic Kenyon cells and b-lobe could be activated extracellularly, and individual bLNs could be activated intracellularly. To elicit STDP, stimuli to KCs and bLNs were paired, forward (dt > 0) or backward (dt < 0), within narrow neurons; a control experiment in temporal windows (630 ms, upper sets of traces). Induction of STDP was sometimes followed which other odorants were paired by injection of octopamine (OCT) into the b lobe (middle trace). The results of these manipula- with the octopamine injection did not tions were tested afterward (bottom traces): STDP facilitated the KC-elicited response in the show this reduction. Since the bLN (rising phase of the EPSP is shown) when dt > 0, and diminished the response when dt < connections b-lobe neurons make 0; delayed delivery of OCT decreased EPSPs elicited only at STDP-tagged synapses (S1). (C) with other b-lobe neurons are In a more naturalistic test, firing in the bLNs elicited by an odor (odor 1) was reduced after that odor specifically (odor 1, but not odor 2) had been paired with OCT injection into the b-lobe. inhibitory, the authors suggested the decrease in spiking associated with octopamine reinforcement would spikes occurred at a favored phase But could STDP contribute to cause the as-yet unidentified position of the oscillatory cycle. associative memory? To test this postsynaptic targets of tagged b-lobe To test whether these responses Cassenaer and Laurent [5] delivered neurons to increase their odor-evoked were consistent with known properties current pulses extracellularly to elicit spiking.
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