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Ground Plan of the Insect Mushroom Body: Functional and Evolutionary Implications

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Ground Plan of the Insect Mushroom Body: Functional and Evolutionary Implications The Journal of Comparative Neurology 513:265–291 (2009) Ground Plan of the Insect Mushroom Body: Functional and Evolutionary Implications 1 2 1 3 NICHOLAS J. STRAUSFELD, * IRINA SINAKEVITCH, SHEENA M. BROWN, AND SARAH M. FARRIS 1Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, Arizona 85721 2IBDML-UMR 6216, Case 907 Parc Scientifique de Luminy, 13288 Marseille Cedex 9, France 3Department of Biology, West Virginia University, Morgantown, West Virginia 26506 ABSTRACT which olfaction is redundant. Examples are cicadas and In most insects with olfactory glomeruli, each side of the mayflies, the latter representing the most basal lineage of brain possesses a mushroom body equipped with calyces winged insects. Mushroom bodies of another basal taxon, supplied by olfactory projection neurons. Kenyon cells pro- the Odonata, possess a remnant calyx that may reflect the viding dendrites to the calyces supply a pedunculus and visual ecology of this group. That mushroom bodies persist lobes divided into subdivisions supplying outputs to other in brains of secondarily anosmic insects suggests that they brain areas. It is with reference to these components that play roles in higher functions other than olfaction. Mush- most functional studies are interpreted. However, mush- room bodies are not ubiquitous: the most basal living in- room body structures are diverse, adapted to different ecol- sects, the wingless Archaeognatha, possess glomerular an- ogies, and likely to serve various functions. In insects whose tennal lobes but lack mushroom bodies, suggesting that the derived life styles preclude the detection of airborne odor- ability to process airborne odorants preceded the acquisi- ants, there is a loss of the antennal lobes and attenuation or tion of mushroom bodies. Archaeognathan brains are like loss of the calyces. Such taxa retain mushroom body lobes those of higher malacostracans, which lack mushroom bod- that are as elaborate as those of mushroom bodies ies but have elaborate olfactory centers laterally in the brain. equipped with calyces. Antennal lobe loss and calycal re- J. Comp. Neurol. 513:265–291, 2009. gression also typify taxa with short nonfeeding adults, in © 2009 Wiley-Liss, Inc. Indexing terms: memory; learning; insect; mushroom bodies; sensory integration; evolution The present account addresses the following question: by neurons from the olfactory lobes. The calyx is a distal what constitutes an insect mushroom body such that its or- neuropil of the mushroom body composed of the dendrites of ganizational ground plan can be reconciled with current mod- this center’s intrinsic neurons (see Fig. 1). In many species of els of its supposed functional properties? The reason why this insects, the calyx is supplied with olfactory input from the brain center must be subject to special scrutiny is in large part antennal lobes, but, in some, it also receives relays from the a result of its acquired reputation as an odorant processor and visual system, and, in one species of gyrinid beetle, visual as a higher brain center that plays a cardinal role in cognition. afferents are the exclusive inputs (Strausfeld, unpublished Common opinion is that mushroom bodies play an indispens- data). The calyx leads to a stalk and a system of lobes that are able role in olfactory discrimination as well as in olfactory formed by the axon-like extensions of intrinsic neurons (see learning and memory (Heisenberg, 1998, 2003; Perez-Orive et Fig. 1). Because for most investigators this organization de- al., 2002; Akalal et al., 2006). The latter is suggested from fines the mushroom body (Flo¨ gel, 1878; Kenyon, 1896; memory deficits caused by targeted disruption of mushroom body development. by suppression of the cyclic AMP cas- cade within its neuropils, or by selective inhibition of protein Grant sponsor: Human Frontiers Science Program; Grant number: signaling or synaptic transmission in its intrinsic neurons, the RG0143/2000-B; Grant sponsor: National Science Foundation; Grant num- ber: IBN 936729; Grant number: IBN9726957; Grant sponsor: National Kenyon cells (deBelle and Heisenberg, 1994; Zars et al., 2000; Institutes of Health NCRR; Grant number: 2-PO1 NS28495-11. McGuire et al., 2001; Ferris et al., 2006). Studies of one N.J.S. and S.M.F. contributed equally to this work. neopteran insect in particular, the locust Schistocerca ameri- *Correspondence to: Dr. Nicholas. J. Strausfeld, ARL Division of Neurobiol- cana, have led to the idea that the mushroom bodies play ogy, 611 Gould-Simpson Bldg., University of Arizona, Tucson, AZ 85721. E-mail: fl[email protected] crucial roles in the encoding and representation of specific Received 27 July 2008; Revised 19 September 2008; Accepted 19 No- odors (Laurent et al., 2001; Cassenaer and Laurent, 2007). vember 2008 However, one problem with these and related studies is that DOI 10.1002/cne.21948 they focus on mushroom bodies that possess a calyx supplied Published online in Wiley InterScience (www.interscience.wiley.com). © 2009 Wiley-Liss, Inc. The Journal of Comparative Neurology 266 N.J. STRAUSFELD ET AL. Figure 1. Summary diagram of the principal elements of mushroom bodies in dicondylic insects. Top: Mushroom bodies with paired calyces (Ca) equipped with Kenyon cells from cell bodies known as globuli cells (gl). Kenyon cells (magenta) have dendritic branches in the calyces, which also receive inputs from sensory neuropils (green): diagrammed here are afferents from the antennal lobes that terminate laterally outside the calyx in the lateral horn neuropil of the protocerebrum (L ho). Afferents and efferents (aff, eff; brown) also supply and extend from various locations in the lobes (see Strausfeld, 2002). Bottom: Calyxless mushroom body with globuli cells (gl) providing Kenyon cells (Kc) with axon-like branches to the vertical and median lobes (V, M). Inputs (afferent; aff) and outputs (efferents; eff) extend to and from various locations along the lobes. Sa´ nchez y Sa´ nchez, 1933), practically all studies over the last The widely held notion that the calyces receive the mush- 3 decades have been interpreted under the assumption that room body’s inputs and its lobes provide its outputs is, how- the calyces alone receive the mushroom body’s inputs and ever, conceptually flawed. Frederick Kenyon in 1896 already the lobes provide its outputs (Menzel, 2001). The general view proposed that other neurons supply terminals to the lobes then is that because Kenyon cell dendrites in the calyces are (Fig. 1). Four recent studies (Ito et al., 1998; Li and Strausfeld, clearly postsynaptic and are the recipients of information 1999; Strausfeld, 2002; Tanaka et al., 2008) unequivocally (Steiger, 1967) their axon-like extensions in the pedunculus demonstrate that, in addition to providing outputs (efferents), and lobes must be overwhelmingly presynaptic, imparting the mushroom body’s lobes receive abundant inputs (affer- information to efferent neurons (Menzel and Manz, 2005; Cas- ents) as well as the aforementioned modulatory neurons. In- senaer and Laurent, 2007). For example, a major role of the deed, if there were no such inputs, the observer would be hard mushroom bodies in mediating learned behaviors in the honey pressed to explain why, in a mushroom body whose calyces bee has been attributed to one type of efferent neuron, called receive almost exclusively olfactory relays, the efferent neu- “Pe1,” recordings from which demonstrate a decrease in re- rons from its lobes can respond to modalities other than sponsiveness as a result of an acquired association of an olfaction, such as acoustic, visual motion, and tactile (Li and olfactory and gustatory stimulus, presumably at the level of Strausfeld, 1997, 1999). Such recordings have been done the calyx (Mauelshagen, 1993; Menzel and Manz, 2005; Okada extensively in cockroaches, where some 14 unique types of et al., 2007). Similarly, it has been proposed that the response efferent neurons responding to a variety of sensory modalities properties of a population of efferents in the locust mushroom have been identified morphologically and functionally. bodies, called “␤-L neurons,” specifically maintain the syn- If it is accepted that mushroom bodies in general give rise to chrony of oscillations that are characteristic of odor represen- efferent neurons that respond to multimodal stimuli, this tations relayed to the calyx (Cassenaer and Laurent, 2007). raises pivotal questions about the basic structure of these Models of how mushroom bodies might function as memory centers and thus their functional organization and evolution. If centers also stress the afferent supply to the calyces as being mushroom body calyces generally receive most of their inputs of crucial importance in associating olfactory stimuli with a from the antennal lobes, what is the role of this specialized conditioned stimulus, either a reward or punishment, that is stream of olfactory input with regard to the mushroom body’s delivered by modulatory neurons that globally innervate the ability to integrate other types of multimodal information re- mushroom body lobes (Schwaerzel et al., 2002, 2007). ceived by its lobes? Furthermore, does the massive innerva- The Journal of Comparative Neurology GROUND PLAN OF THE INSECT MUSHROOM BODY 267 tion of the mushroom body calyx by olfactory afferents in feld et al., unpublished data). We argue that this organization, phylogenetically divergent species, such as the locust, cock- which represents the Zygentoma
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