View metadata, citation and similar papers at core.ac.uk brought to you by CORE

provided by Elsevier - Publisher Connector Dispatch R493

leaf-feeding herbivores, bees may and response systems, or the retention natural ligands for Drosophila olfactory receptor neurones. J. Exp. Biol. 206, 715–724. have little need for the bitter taste of adaptive mechanisms evolved in 11. de Bruyne, M., and Baker, T.C. (2008). Odor receptors that other phytophagous ancestral environments. A comparative detection in insects: volatile codes. J. Chem. insects use to detect these approach employing the analytical Ecol. 34, 882–897. 12. Nottingham, S.F., Hardie, J., Dawson, G.W., compounds [19]. tools discussed here may soon answer Hick, A.J., Pickett, J.A., Wadhams, L.J., and While sericulture is not as ancient such questions, while perhaps also Woodcock, C.M. (1991). Behavioral and electrophysiological responses of aphids to as the relationship between bees teaching us how to manipulate such host and nonhost plant volatiles. J. Chem. and flowers, silkworms were being interactions to enhance the sustainable Ecol. 17, 1231–1242. cultured in China by 2500 B.C. and management of agricultural 13. Fraser, A.M., Mechaber, W.L., and Hildebrand, J.B. (2003). Electroantennographic probably much earlier. The potential ecosystems. and behavioral responses of the sphinx moth for evolutionary change over this Manduca sexta to host plant headspace period is amply demonstrated by the volatiles. J. Chem. Ecol. 29, 1813–1833. References 14. Visser, J.H. (1986). Host odour perception in phytophagous insects. Annu. Rev. Entomol. adults of B. mori, which have lost the 1. Touhara, K., and Vosshall, L.B. (2009). Sensing 31, 121–144. ability to fly and do not feed. Moreover, odorants and pheromones with chemosensory 15. Tanaka, K., Uda, Y., Ono, Y., Nakagawa, T., receptors. Annu. Rev. Physiol. 71, 307–332. while adult B. mori express BmOr-56 Suwa, M., Yamaoka, R., and Touhara, K. (2009). 2. Farmer, E.E. (2001). Surface-to-air signals. Highly selective tuning of a silkworm olfactory they do not respond to cis-jasmone Nature 411, 854–856. receptor to a key mulberry leaf volatile. 3. De Moraes, C.M., Mescher, M.C., and or, apparently, to any odor cues apart Curr. Biol. 19, 881–890. Tumlinson, J.H. (2001). Caterpillar-induced 16. Loughrin, J.H., Manukian, A., Heath, R.R., and from the sex pheromone, bombykol, nocturnal plant volatiles repel conspecific Tumlinson, J.T. (1995). Volatiles emitted by which still guides reproduction. But, females. Nature 410, 577–580. different cotton varieties damaged by feeding 4. De Moraes, C.M., Lewis, W.J., Pare´ , P.W., and though an intriguing possibility, it is beet armyworm larvae. J. Chem. Ecol. 21, Tumlinson, J.H. (1998). Herbivore infested 1217–1227. currently impossible to say whether plants selectively attract parasitoids. Nature 17. Bruce, T.J.A., Matthes, M.C., Chamberlain, K., 393, 570–574. the simplicity of the observed Woodcock, C.M., Mohib, A., Webster, B., 5. Rasmann, S., Kollner, T.G., Degenhardt, J., Smart, L.E., Birkett, M.A., Pickett, J.A., and response of domesticated B. mori Hiltpold, I., Toepfer, S., Kuhlmann, U., Napier, J.A. (2008). cis-Jasmone induces larve to olfactory cues from their Gershenzon, J., and Turlings, T.C.J. (2005). Arabidopsis genes that affect the chemical Recruitment of entomopathogenic nematodes host plant reflects the reduction of ecology of multitrophic interactions with aphids by insect-damaged maize roots. Nature 434, and their parasitoids. Proc. Natl. Acad. Sci. a more complex suite of responses 732–737. USA 105, 4553–4558. 6. Seybold, S.J., Huber, D.P.W., Lee, J.C., employed by the free-living ancestors. 18. Becher, P.G., and Guerin, P.M. (2008). Oriented Graves, A.D., and Bohlmann, J. (2006). Pine responses of grapevine moth larvae Lobesia To answer this question, it would be monoterpenes and pine bark beetles: botrana to volatiles from host plants and an very useful to investigate the olfaction a marriage of convenience for defense and artificial diet on a locomotion compensator. chemical communication. Phytochem. Rev. and behavior of adults and larvae of J. Insect Physiol. 55, 384–393. 5, 143–178. 19. Robertson, H.M., and Wanner, K.W. (2006). B. mandarina, the nearest wild relative 7. Bruce, T.J.A., Wadhams, L.J., and The chemoreceptor superfamily in the honey Woodcock, C.M. (2005). Insect host location: of B. mori. bee, Apis mellifera: Expansion of the odorant, a volatile situation. Trends Plant Sci. 10, but not gustatory, receptor family. Genome What is clear from the new study [15], 269–274. Res. 16, 1395. however, is the power of the approach 8. Baker, T.C., Fadamiro, H.Y., and Cosse, A.A. employed here to reveal patterns of (1998). Moth uses fine tuning for odour resolution. Nature 393, 530. 1 2 olfactory reception and response that 539 and 535 ASI Building Center, Chemical 9. Blight, M.M., Pickett, J.A., Wadhams, L.J., and Ecology, Penn State University, bear directly on such questions by Woodcock, C.M. (1995). Antennal perception of oilseed rape, Brassica napus (Brassicaceae), University Park, PA 16802, USA. integrating genomic, ecological, and volatiles by the cabbage seed weevil E-mail: [email protected], czd10@psu. physiological data. The convergence Ceutorhynchus assimilis (Coleoptera: edu of these empirical approaches Curculionidae). J. Chem. Ecol. 21, 1649–1664. 10. Stensmyr, M.C., Giordano, E., Balloi, A., promises to provide new insights Angioy, A.M., and Hansson, B.S. (2003). Novel DOI: 10.1016/j.cub.2009.05.011 into the ecological significance of volatile-mediated interactions among plants and insects, and into their evolutionary origins, which are currently little known. To that end, exploration of differences between : Saccadic natural and human-dominated (for example, agricultural) systems, as Omission — Suppression suggested above for B. mori, may be a valuable starting point for future or Temporal Masking? work. A surprising aspect of much past work in plant–insect chemical ecology Although we don’t perceive visual stimuli during saccadic eye movements, new is the frequent documentation of evidence shows that our brains do process these stimuli and they can influence complex and sophisticated our subsequent visual perception. interactions — mediated by plant volatiles — occurring in agricultural assemblages of plant and insect Michael R. Ibbotson essential for pointing the eye at species that do not reflect natural and Shaun L. Cloherty targets in the scene, they induce associations. It is often not clear rapid and potentially disturbing visual whether such apparent adaptation People shift their between motion across the . Yet in reflects rapid evolution of insect objects of interest using rapid everyday experience these rapid olfactory responses in these systems, pre-planned eye movements known scene shifts are not perceived. In fact, inherent flexibility in insects’ detection as saccades. While saccades are most visual stimuli presented just Current Biology Vol 19 No 12 R494

Figure 1. Saccadic omission. (A) Photograph of a flight of steps overlayed with a typical trajectory. The first fixation, X, is on a low contrast step. A saccade is then made across a high contrast riser, Y, and re-fixation occurs on a low contrast step, Z. (B) Schematic illustration of neural responses from a visual neuron, without saccadic modulation, around the time of the saccade. There is low-level ongoing activity during fixation at X (black), the response to Y is large (blue) and the response to Z is small (red). (C) The same schematic illustration of neural responses with saccadic modulation. Ongoing activity is suppressed around saccade start at X. The response to Y is suppressed (blue response; black dashed line indicates the unmodulated response) and the response at re-fixation, Z, is greatly enhanced (red response; black dashed line shows the unmodulated response). Also, the response latencies to stimulation at Y and Z are reduced, thus trun- cating the blue response. The re-fixation response far exceeds the response during the saccade even though the stimulus strength is weak, thus promoting backward temporal masking. (D) Mean response amplitudes around the time of saccades from 72 MST neurons in two macaque monkeys (for experi- mental procedures see [13]). Response ampli- tudes for stimuli delivered prior to the saccade are suppressed compared to the control level at unity while responses to stimuli delivered after the saccade are enhanced. Coloured bars indicate periods of significant suppres- sion (blue) and enhancement (red) (t-test, p < 0.01, n = 72). Representative responses from a single neuron are shown at the bottom of the figure. The yellow bar shows the saccade duration.

stimuli cannot be attributed solely to saccadic suppression, because visual stimuli are evidently processed by the before and during saccades are not saccades but that the mechanism during saccades. This finding perceived [1], a phenomenon referred of saccadic omission prevents is consistent with previous to as saccadic omission. As reported such processing from reaching observations suggesting that in this issue of Current Biology, perception. suppression is not sufficient to fully Watson and Krekelberg [2] employed A debate has raged for many explain the mechanism of saccadic a visual shape illusion to probe the years about how the visual system omission [6]. Backward masking mechanism underlying saccadic perceptually ‘omits’ visual stimuli would therefore appear to offer omission. In brief, presentation of an during saccades [1,2,4–6]. One a plausible mechanism for saccadic inducing stimulus (an oriented line) theory suggests that, in planning to omission. But backward masking distorts the perceived shape of make a saccade, the brain relies on the mask being stronger a subsequently presented circle [3]: simultaneously sends signals to than the stimulus during the antecedent when the line is presented the suppress the visual pathways [1]. saccade [7]. Therefore, a visual circle appears oval-shaped. When An alternative theory suggests that stimulus during the saccade would the inducing stimulus was presented saccadic omission is the result of need to be weak compared to the visual just before a saccade, the observers backward temporal masking, stimulus at re-fixation. The problem is were not aware of it, but when the whereby visual stimuli present at that in natural scenes this requirement circle was presented after the the time of re-fixation overpower, or is frequently challenged. saccade the observers still mask, stimuli presented before or Consider the example illustrated in perceived an oval. The implication during the saccade [4–6]. Watson Figure 1A. The horizontal surfaces of is that the visual brain continues to and Krekelberg’s [2] experiments the steps have little contrast and process visual information during suggest that omission of pre-saccadic provide only weak visual stimulation; Dispatch R495 however, the risers between steps shorter latencies in Figure 1C stimuli are omitted from awareness, have high contrast and provide compared to 1B). The elegance of yet some visual processing capacity strong visual stimulation. For this unifying theory is that it obviates is retained. Rather than suppressing a saccade made from one step to the need for absolute suppression everything during a saccade, the the next (from X to Z) the visual of neural activity — visual processing visual system is geared towards stimulus during the saccade would can persist during the saccade enhancing what happens after it. be strong while the mask stimulus provided the enhanced response to This simultaneously generates at saccade-end would be weak. the stimulus at re-fixation is powerful backward masking and Neural responses for this scenario, sufficient to invoke backward promotes important information at assuming no saccadic modulation, masking and hence dominate re-fixation. Also, based on the are illustrated schematically in perception. observations by Watson and Figure 1B. It seems unlikely that This theory is contingent upon Krekelberg [2], perception at re-fixation backward masking could adequately substantial post-saccadic is formed in the context of the deal with this common visual (re-fixation) enhancement, rather information coded during the planning situation, as the response during the than the pre-saccadic suppression, and execution of the saccade. saccade is dominant. of neural responses. This is Evidently, neither suppression consistent with the available References 1. Ross, J., Morrone, M.C., Goldberg, M.E., and of neural activity nor backward physiological evidence — while Burr, D.C. (2001). Changes in visual perception temporal masking alone can fully saccadic suppression of neural at the time of saccades. Trends Neurosci. 24, explain the phenomenon of activity is reportedly weak in many 113–121. 2. Watson, T.L., and Krekelberg, B. (2009). The saccadic omission. However, recent brain areas [4,8,9], post-saccadic relationship between saccadic suppression physiological experiments in enhancement is a robust and and perceptual stability. Curr. Biol. 19, 1040–1043. behaving primates may provide a prominent feature of all areas 3. Suzuki, S., and Cavanagh, P. (1998). A unifying theory. In primates, there investigated to date [4,13]. Moreover, shape-contrast effect for briefly presented is a biphasic modulation of visual this hypothesis is also consistent stimuli. J. Exp. Psychol. Hum. Percept. Perform. 24, 1315–1341. sensitivity around the time of with the behavioural evidence 4. Wurtz, R.H. (2008). Neuronal mechanisms of saccades [8–13]. This consists of a presented in Watson and Krekelberg visual stability. Vision Res. 48, 2070–2089. 5. Campbell, F.W., and Wurtz, R.H. (1978). pre-saccadic reduction and a [2] — evidently, the pre-saccadic Saccadic omission: why we do not see substantial post-saccadic inducing stimulus is omitted from a grey-out during a saccadic eye movement. enhancement of spontaneous awareness, possibly by backward Vision Res. 18, 1297–1303. 6. Castet, E., Jeanjean, S., and Masson, G.S. neural activity and visual sensitivity. masking, yet this same stimulus is (2002). Motion perception of saccade-induced In the medial superior temporal area clearly processed to some extent by retinal translation. Proc. Natl. Acad. Sci. USA 99, 15159–15163. (MST) of the parietal cortex, for example, the brain and, importantly, can 7. Breitmeyer, B.G., and Ogmen, H. (2000). the mean pre-saccadic reduction in influence the perception of Recent models and findings in visual visual sensitivity is around 50% and subsequent visual stimuli. backward masking: a comparison, review, and update. Perc. Psychophys. 62, 1572–1595. the post-saccadic (or re-fixation) In primates, most visual information is 8. Reppas, J.B., Usrey, W.M., and Reid, R.C. enhancement boosts responses by relayed via the lateral geniculate (2002). Saccadic eye movements modulate visual responses in the lateral geniculate more than 70% (Figure 1D) [13]. nucleus (LGN) to the primary visual nucleus. Neuron 35, 961–974. Consider now a saccade from X to cortex (V1) and then through two major 9. Royal, D.W., Sary, G., Schall, J.D., and Z, as shown in Figure 1A, but in the cortical pathways: the ventral and Casagrande, V.A. (2006). Correlates of motor planning and postsaccadic fixation in the context of this biphasic modulation dorsal streams. In the early visual macaque monkey lateral geniculate nucleus. of visual sensitivity. The initial system (LGN and V1), saccadic Exp. Brain Res. 168, 62–75. 10. Kagan, I., Gur, M., and Snodderly, D.M. (2008). suppression would reduce the suppression is weak [4,8–11]. Therefore, Saccades and drifts differentially modulate visibility of the high contrast stimulus pre-saccadic stimuli almost certainly neuronal activity in V1: Effects of retinal image during the saccade while neural enter both cortical pathways. In the motion, position, and extraretinal influences. J. Vision 8, 19.1–25. responses to the weak stimulus at dorsal pathway, physiological studies 11. Rajkai, C., Lakatos, P., Chen, C.-M., Pincze, Z., re-fixation would be enhanced show that, although suppression is Karmos, G., and Schroeder, C.E. (2008). Transient cortical excitation at the onset of (Figure 1C). In effect, although the widespread (Figure 1D), some visual fixation. Cereb. Cortex 18, 200–209. mask stimulus itself is weak, the processing of visual information 12. Ibbotson, M.R., Price, N.S.C., Crowder, N.A., response to the mask is strong. continues during saccades [14,16]. Ono, S., and Mustari, M.J. (2007). Enhanced motion sensitivity follows saccadic Thus, the biphasic modulation of Little is known about saccadic suppression in the superior temporal sulcus visual sensitivity could potentiate modulation of neural activity in the of the macaque cortex. Cereb. Cortex 17, 1129–1138. the efficacy of backward masking. ventral pathway [17,18]. The available 13. Ibbotson, M.R., Crowder, N.A., Cloherty, S.L., Moreover, recent studies in psychophysical evidence suggests that Price, N.S.C., and Mustari, M.J. (2008). monkeys [12–15] have shown that processing of some stimulus attributes Saccadic modulation of neural responses: possible roles in saccadic suppression, the latencies of responses to in the ventral stream is not suppressed enhancement and time compression. post-saccadic stimuli are reduced during saccades [2,19,20]. Addressing J. Neurosci. 28, 10952–10960. 14. Price, N.S.C., Ibbotson, M.R., Ono, S., and compared to those for the same the lack of evidence pertaining to Mustari, M.J. (2005). Rapid processing of retinal stimulus presented before saccadic modulation of neural activity slip during saccades in macaque area MT. a saccade. Thus, responses to the in the ventral stream is the next J. Neurophysiol. 94, 235–246. 15. Ibbotson, M.R., Crowder, N.A., and post-saccadic mask stimulus could major step towards understanding Price, N.S.C. (2006). Neural basis of time truncate the saccadic response saccadic omission. changes around the time of saccades. Curr. Biol. 16, R834–R836. and further enhance the backward In summary, visual processing 16. Thiele, A., Henning, P., Kubischik, M., and masking mechanism (note the during saccades is complex. Saccadic Hoffmann, K.-P. (2002). Neural mechanisms Current Biology Vol 19 No 12 R496

of saccadic suppression. Science 295, suppression in humans. Curr. Biol. 14, Visual Sciences, Group and ARC Centre 2460–2462. 386–390. of Excellence in Vision Science, 17. Tolias, A.S., Moore, T., Smirnakis, S.M., 19. Burr, D.C., Morrone, M.C., and Ross, J. (1994). Australian National University, Canberra, Tehovnik, E.J., Siapas, A.G., and Schiller, P.H. Selective suppression of the magnocellular (2001). Eye movements modulate visual visual pathway during saccadic eye ACT 2601, Australia. receptive fields of V4 neurons. Neuron 29, movements. Nature 371, 511–513. E-mail: [email protected] 757–767. 20. Diamond, M.R., Ross, J., and Morrone, M.C. 18. Kleiser, R., Seitz, R.J., and Krekelberg, B. (2000). Extraretinal control of saccadic (2004). Neural correlates of saccadic suppression. J. Neurosci. 20, 3449–3455. DOI: 10.1016/j.cub.2009.05.010

Antigenic Variation: Extending the silencing in the malaria parasite [7]. These results also indicated that the Reach of Telomeric Silencing silencing effect can spread great distances from the telomere. In the trypanosome, however, disruption of Immune evasion in the parasitic African trypanosome relies upon the silencing tbSIR2 resulted in only partial loss of of variant surface glycoprotein genes that are found adjacent to telomeres. silencing close to the telomere and Work on the RAP1 telomere-binding protein now indicates that silencing VSG ES promoters were unaffected spreads over a sufficient distance to repress these genes. [12] (Figure 1A). So how are telomeric VSG genes David Horn trypanosomes, the VSG coats the cell silenced? Telomere position effects and has the capacity to shield other that are mechanistically related to Promoters drive gene expression by surface molecules from immune attack those described in yeast have obvious recruiting RNA polymerase but, in the [4]. There are many potential telomeric appeal and sequencing of the vicinity of telomeres, promoters and VSG expression sites (ESs; Figure 1) trypanosome genome presented new their associated genes are silenced. but only a single VSG is expressed by opportunities for research in this area. This ‘telomere position effect’ each cell and a co-ordinated switch can Yang and colleagues [3] now provide phenomenon was first described in transfer active transcription from one direct evidence that telomeres are yeast [1] and was subsequently telomere to another [5]. Importantly, involved in the regulation of VSG demonstrated in human cells and also silencing at all other ESs is critical to control by showing that depletion of in trypanosomes [2]. There are distinct maintain monoallelic expression and trypanosome RAP1 increases VSG types of telomeric silencing that are the integrity of the evasion strategy. expression from all ESs by up to mediated by different factors and, The discovery of telomeric silencing 50-fold (Figure 1B,C). tbRAP1 was depending upon the cell type, differ offered a potential mechanism for the initially identified via an interaction in the distance that the effect spreads control of VSG genes in trypanosomes, with a telomere repeat-binding factor from the telomere. A recent study on as well as for the control of other (tbTRF1) and was then shown to the trypanosome telomere-binding subtelomeric gene families that are colocalise with this protein and to protein repressor/activator protein 1 subject to monoallelic expression, associate with telomeric DNA, possibly (RAP1) now reveals that a far-reaching such as those encoding olfactory directly via Myb-like DNA-binding type of silencing extends over receptors in mammals [6] and variant domains. Depletion of tbRAP1 using a sufficient distance to silence all but surface proteins (var genes) in the an inducible RNA interference one of the promoters associated with malaria parasite [7]. Crucially, the approach indicated that the protein variant surface glycoprotein (VSG) silencing effect would have to extend is essential for growth but provided genes [3]. a long way from the telomere in these a window of opportunity to explore The African trypanosome, organisms if these genes were to be VSG expression. To provide good Trypanosoma brucei, is a protozoan affected. Most of what we know about coverage, the authors exploited parasite of major medical and telomeric silencing mechanisms a recently published complement economic importance. These highly comes from studies in yeast where of ES sequences [13] and used motile cells circulate in the mammalian the repressive activity of RAP1 is quantitative real-time PCR to examine host bloodstream and are spread exhibited at telomeres [8], via binding the expression of all fourteen VSGs among mammals by tsetse flies. to the characteristic short telomeric located in telomeric ESs in the strain Mammalian host immune mechanisms DNA repeats and recruitment of analysed. Importantly, VSG-specific will likely eliminate any infectious a silent information regulator (SIR) antisera detected multiple VSGs on agent that exposes a common set complex. This SIR complex spreads the surface of individual cells following of epitopes for several days and this beyond the telomeric repeats and tbRAP1 depletion, indicating that is why many pathogens have evolved modifies histones, thus forming silent monoallelic VSG expression was strategies for phenotypic, clonal chromatin or heterochromatin at severely compromised. Other recent variation of surface proteins. African subtelomeres [9]. The SIR2 component studies support the idea that multiple trypanosomes provide a sophisticated of this complex is a histone chromatin modifiers cooperate to example of an immune evasion deacetylase [10], and disruption of silence VSG ESs; deletion of a histone strategy that allows the establishment SIR2-related proteins results in loss methyltransferase gene (tbDOT1B, of a persistent infection in of telomeric gene silencing in yeast named after yeast disruptor of immunocompetent hosts. In [11] and loss of telomeric var gene telomeric silencing 1, DOT1) led to