Olfaction and Olfactory Learning in Drosophila: Recent Progress Andre´ Fiala
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Olfaction and olfactory learning in Drosophila: recent progress Andre´ Fiala The olfactory system of Drosophila resembles that of experience. For example, an odor repetitively paired with vertebrates in its overall anatomical organization, but is a food reward becomes attractive. Conversely, an odor considerably reduced in terms of cell number, making it an ideal that often occurs concurrently with a punishment model system to investigate odor processing in a brain becomes a predictor for a negative situation and will be [Vosshall LB, Stocker RF: Molecular architecture of smell avoided. Drosophila melanogaster can easily perform such and taste in Drosophila. Annu Rev Neurosci 2007, 30:505- learning tasks and represents an excellent organism to 533]. Recent studies have greatly increased our knowledge investigate the neuronal mechanisms underlying such about odor representation at different levels of integration, from olfactory learning processes for two reasons. First, con- olfactory receptors to ‘higher brain centers’. In addition, siderable progress has already been made during recent Drosophila represents a favourite model system to study the years in analyzing how odors are represented in the fly’s neuronal basis of olfactory learning and memory, and brain [1]. Second, the powerful genetic techniques by considerable progress during the last years has been made in which structure and function of identified neurons can be localizing the structures mediating olfactory learning and observed and manipulated makes Drosophila an ideal memory [Davis RL: Olfactory memory formation in neurobiological model system to characterize a neuronal Drosophila: from molecular to systems neuroscience. Annu network that mediates olfactory learning and memory [2– Rev Neurosci 2005, 28:275-302; Gerber B, Tanimoto H, 4]. The scope of this review is to summarize recent Heisenberg M: An engram found? Evaluating the evidence advances and to point out gaps and caveats in our current from fruit flies. Curr Opin Neurobiol 2004, 14:737-744; Keene understanding of olfactory coding and olfactory learning AC, Waddell S: Drosophila olfactory memory: single genes in Drosophila. to complex neural circuits. Nat Rev Neurosci 2007, 8:341- 354]. This review summarizes recent progress in analyzing Olfactory representations in the Drosophila olfactory processing and olfactory learning in Drosophila. brain Fruitflies perceive odors through olfactory sensory neurons Addresses (OSNs) that reside in sensillae of diverse morphological Department of Genetics and Neurobiology, Theodor-Boveri-Institut, Julius-Maximilians-Universita¨ tWu¨ rzburg, Biozentrum, Am Hubland, types on the third antennal segments and the maxillary 97074 Wu¨ rzburg, Germany palps. Each of these sensory neurons expresses usually one, but sometimes two or three out of 61 specific olfactory Corresponding author: Fiala, Andre´ receptor proteins (ORs). In addition, the non-specific re- (afi[email protected]) ceptor Or83b is expressed in almost all olfactory sensory neurons and mediates targeting and functionality of the Current Opinion in Neurobiology 2007, 17:720–726 heterodimers it forms with the odor-selective receptor [5– 7]. The principle of connecting the OSNs to the brain is This review comes from a themed issue on simple: OSNs expressing the same ORs converge onto one Neurobiology of behaviour Edited by Edvard Moser and Barry Dickson or very few out of 40–50 spherical synaptic modules, the glomeruli of the antennal lobe [8,9]. Available online 1st February 2008 0959-4388/$ – see front matter The response profiles of these OSNs are reflected in the # 2007 Elsevier Ltd. All rights reserved. range of volatile compounds with which their ORs interact. Some of the ORs are highly specialized with respect to DOI 10.1016/j.conb.2007.11.009 their response profile. For example, the two receptors Gr21a and Gr63a which actually belong to the family of gustatory receptors are co-expressed in the same antennal Introduction OSNs. These neurons target one specific glomerulus, the Animals such as fruitflies navigate in a complex chemo- V-glomerulus [10] and mediate very specifically the fly’s sensory environment. Some odors can act as signals for olfactory detection of CO2 [10–12]. Artificial activation of food or danger or as pheromones released by conspecifics just these neurons using the light-sensitive cation channel eliciting innate behavioral responses. However, many ‘channelrhodopsin-2’ is sufficient to induce the fly’s very odor stimuli are not informative per se to optimally guide pronounced avoidance response normally elicited by CO2 the animal’s behavior. The brain has to make sense of the [13]. complexity of odor signals by interpreting their relevance. Associative learning represents one process by which new In contrast to such an odor selectivity among fruitfly OR or altered relevance is assigned to a stimulus through subtypes, other ORs can be more broadly activated by a Current Opinion in Neurobiology 2007, 17:720–726 www.sciencedirect.com Odor learning in Drosophila Fiala 721 variety of volatiles. For example, the response range of vioral responses cannot be deduced from the knowledge OSNs expressing one particular receptor (Or22a), ana- of combinatorial OR activations and inhibitions. Rather, lysed in a detailed calcium imaging study by Pelz et al. processing of olfactory information might alter the [14], covers 39 out of 104 tested odorants. However, the particular contribution of defined OSNs to the ultimate calcium response evoked by ethyl hexanoate and methyl behavior-releasing effect of an odor. hexanoate, components of several fruit odors, clearly exceeded those evoked by the other volatiles tested. A In fact, the antennal lobe comprises a complex network of systematic analysis of 24 odorant receptors has been several types of neurons. Around 150, mostly uniglomer- reported in an impressive and very comprehensive study ular, olfactory projection neurons (PNs) in each hemi- by Hallem and Carlson [15], expanding results from a sphere receive inputs from 1300 OSNs and convey odor previous publication [16]. Here, the authors misexpressed information from the antennal lobe to the lateral horn and the different ORs in a neuron that lacks its endogenous the mushroom body, but provide also local output within receptor and recorded electrophysiologically neuronal the antennal lobe. Multiglomerular local interneurons activity in the corresponding sensillum evoked by 110 which are diverse with respect to their transmitter project different volatiles across various concentrations. This throughout large parts of the antennal lobe. Inhibitory study revealed that a sharp division into generalist and actions mediated by GABAergic local neurons shape the specialist receptors cannot be actually made. Rather, PN responses [18]. More recently, excitatory, cholinergic tuning breadths of ORs are variable, with some receptors interneurons have also been found that broaden the being activated by one or very few compounds, others response spectra of individual PNs [19,20]. The net effect responding to a wide variety of compounds, and a con- of these processing circuits has been subject to a con- tinuum of response spectra in between. In addition, troversial discussion. Whereas optical imaging studies inhibition of a receptor by a particular odorant occurs have suggested that the antennal lobe’s input provided relatively often, demonstrating that odor representations via OSNs is essentially mirrored by PN output [21,22], at this initial level of processing are characterized by both electrophysiological studies have indicated a more com- excitation and inhibition of particular OSNs. Taken plex transformation of odor information [23]. A recent together, these studies offer the fascinating prospect that publication by Bandhavat et al. [24] clearly demon- a nearly complete knowledge of possible OSN responses strates that response spectra of PNs receiving their main providing odor information to the fly’s brain is within input from ‘non-specialist’ OSNs are considerably reach. Moreover, as OSNs expressing the same ORs broader compared to their input counterparts. Interest- target the same identified glomeruli in the antennal lobe, ingly, the odorant evoking the strongest activity in a one can create a map of odotopic representations in this particular OSN is not necessarily the most efficient odor primary olfactory neuropil. Two laboratories have started to activate its corresponding PN [24]. doing just that [8,9]. By tracing the projections of sensory neurons to their antennal lobe targets a detailed receptor- PNs transmit olfactory information to the lateral horn, a to-glomerulus map has been proposed. This anatomical brain region whose exact mode of function is not well connectivity scheme could be combined with the already understood. Most of the PNs also target en passent the established response profiles of ORs to provide the first calyx, the main olfactory input region of the mushroom framework for a functional atlas of the antennal lobe [8,9]. body. The mushroom body of each hemisphere consist of 2500 intrinsic neurons, the Kenyon cells, which can be These advances made over the last years have led to a divided into various classes due to their birth order, gene more and more comprehensive description of the periph- expression and axonal projections: early a/b-, late a/b-, eral mechanisms underlying the ‘odor space’ of a fly. a0/b0- and g-neurons. Several anatomical studies have However, little information is available