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7. Godefroit, P., Cau, A., Dong-Yu, H., Escuillie´ , F., 11. Lee, M.S.Y., Cau, A., Naish, D., and Dyke, G.J. 17. Erickson, G.M., Rauhut, O.W., Zhou, Z., Wenhao, W., and Dyke, G. (2013). A Jurassic (2014). Sustained miniaturization and Turner, A.H., Inouye, B.D., Hu, D., and avialan dinosaur from China resolves the early anatomical innovation in the dinosaurian Norell, M.A. (2009). Was dinosaurian physiology phylogenetic history of birds. Nature 498, ancestors of birds. Science 345, 562–566. inherited by birds? Reconciling slow growth in 359–362. 12. Benson, R.B.J., Campione, N.E., Carrano, M.T., Archaeopteryx. PLoS One 4, e7390. 8. Brusatte, S.L., Vremir, M., Csiki-Sava, Z., Mannion, P.D., Sullivan, C., Upchurch, P., and 18. Clarke, J.A. (2013). Feathers before flight. Turner, A.H., Watanabe, A., Erickson, G.M., and Evans, D.E. (2014). Rates of dinosaur Science 340, 690–692. Norell, M.A. (2013). The osteology of Balaur body mass evolution indicate 170 million 19. Longrich, N.R., Tokaryk, T., and Field, D.J. bondoc, an island-dwelling dromaeosaurid years of sustained ecological innovation (2011). Mass extinction of birds at the (Dinosauria: Theropoda) from the Late on the avian stem lineage. PLoS Biol. 12, Cretaceous-Paleogene boundary. Proc. Natl. Cretaceous of Romania. Bull Am. Museum e1001853. Acad. Sci. USA 108, 15253–15257. Natural History 374, 1–100. 13. Puttick, M.N., Thomas, G.H., and Benton, M.J. 20. Mitchell, J.S., and Makovicky, P.J. (2014). Low 9. Makovicky, P.J., Apesteguı´a, S., and (2014). High rates of evolution proceeded the ecological disparity in Early Cretaceous birds. Agnolı´n, F.L. (2005). The earliest origin of birds. Evolution 68, 1497–1510. Proc. R. Soc. B. Biol. Sci. 281, 20140608. dromaeosaurid theropod from South America. 14. Sereno, P.C. (1999). The evolution of dinosaurs. Nature 437, 1007–1011. Science 284, 2137–2147. 10. Norell, M.A., Clark, J.M., and Makovicky, P.J. 15. Turner, A.H., Pol, D., Clarke, J.A., Bruce Museum, 1 Museum Drive, Greenwich, (2001). Phylogenetic relationships among Erickson, G.M., and Norell, M.A. (2007). A basal CT 06830, USA. coelurosaurian theropods. In New Perspectives dromaeosaurid and size evolution preceding on the Origin and Early Evolution of Birds, avian flight. Science 317, 1378–1381. E-mail: [email protected] J. Gauthier and L.F. Gall, eds. (New Haven: 16. Balanoff, A.M., Bever, G.S., Rowe, T.B., and Peabody Museum of Natural History), Norell, M.A. (2013). Evolutionary origins of the pp. 49–68. avian brain. Nature 501, 93–96. http://dx.doi.org/10.1016/j.cub.2014.09.018

Vision: Melanopsin as a Novel elegant approach that combines the use of a genetically modified mouse, Irradiance Detector at the Heart where the spectral sensitivity of cones has been long-wavelength shifted, of Vision together with metameric silent substitution to probe the impact of selectively activating or not activating A recent study defines a novel role of melanopsin-expressing ipRGCs, showing melanopsin during the presentation that these inner retinal photoreceptors function as retinal irradiance detectors of photopic visual stimuli. Allen et al. and provide a local measure of luminance to regulate functional adaptation in convincingly show reversible changes the mammalian retina. in the photopic flash electroretinogram (ERG) between ‘daylight’ and ‘mel-low’ Mark W. Hankins* and Steven Hughes pathway and explore the mechanisms lighting conditions — lighting of luminance-dependent adaptation in conditions that activate both classes The photopigment melanopsin (Opn4) the retina, a feature that is fundamental of cones equally but differ significantly has come a long way since the end of to visual function. For many years it in their activation of melanopsin (while the last century. What began as a quest was naturally assumed that all light largely saturating rod responses). to identify the circadian photoreceptor detection in the retina was driven by Under daylight conditions cone ERG critically led to the discovery of a new rod and cone photoreceptors, so that responses are reduced at high light class of inner retinal photoreceptor the mechanisms that regulate both intensities, but this adaptive response comprising a population of retinal photoreceptor and retinal network is lacking under mel-low conditions ganglion cells that are intrinsically adaptation were assumed to be driven where activation of melanopsin photosensitive (ipRGCs) [1–3]. These by these same cells. The emergence is selectively reduced. Critically, ipRGCs express Opn4 [4], a blue light of inner-retinal photoreceptors simultaneous recording in the dorsal sensitive opsin protein capable of essentially overthrew this dogma lateral geniculate nucleus (dLGN) rendering cells intrinsically light and raised the possibility that some revealed changes in feature selectivity responsive [5]. In the decade that of these systems are driven by of visual circuits in both temporal and followed their discovery, we have learnt melanopsin-expressing ipRGCs. The spatial dimensions depending on levels a lot about melanopsin cells and how first piece of evidence that this might of melanopsin activation. A substantial they provide photic input to the be the case came from a study of fraction of units preferred finer spatial suprachiasmatic nucleus (SCN) and human vision, where it was first patterns in the daylight condition, while other retino-recipient areas demanding shown that a diurnal rhythm in the the population of direction-sensitive of a robust and highly reliable measure human cone electroretinogram (ERG) units became tuned to faster motion. of irradiance. It has been widely was regulated by a photoreceptor with By studying the responses to simple assumed that such an irradiance signal a melanopsin-like spectral sensitivity movies they conclude that the dLGN is required by the SCN, principally [6]. Melanopsin was later shown to contained a richer encoding of natural because rod and cone photoreceptors be critical in the diurnal and circadian scenes when melanopsin was show profound levels of adaption regulation of the mouse photopic activated. to background light levels and are ERG [7]. What are the implications of these themselves an unreliable reporter of In their latest work, reported in this phenomena to vision? It has become overall environmental light levels. issue of Current Biology, Allen et al. clear that visual coding is a highly Following this analogy it becomes [8] present new data on the role of dynamic process and is continuously interesting to revisit the classical visual melanopsin in vision, employing an adapting to the current viewing context Current Biology Vol 24 No 21 R1056

Figure 1. Interactions between melanopsin ipRGCs and central visual pathways. (A) Cross-section image showing the location and anatomy of cone photoreceptors (green) and different ipRGC subtypes (red) of the mouse retina. M1 ipRGCs express high levels of melanopsin and have dendrites (white arrows) located in the OFF layer of the IPL. M2 ipRGCs express lower levels of melanopsin and their dendrites stratify the ON layers of the IPL (dotted white arrows). Displaced M1 ipRGCs are located within the inner nuclear layer, and in this case can be seen to extend processes towards the outer retina (asterisk) — a feature only rarely observed for ipRGCs. (B,C) Collectively, M1–M5 ipRGCs innervate a range of non-image forming areas of the brain including the SCN (almost exclusively M1 ipRGCs [2]), and also innervate a number of visual centres including the dLGN (predominately M4 ipRGCs [13]). ipRGCs labelled using a highly characterised anti-melanopsin antibody (UF006); cones labelled using anti-b-gal antibodies following transgenic insertion of a LacZ reporter cassette within the SWS1 locus (unpublished data). DAPI nuclear counter stain shown in blue. Retino-recipient areas of M1–M5 type ipRGCs identified using an Opn4. Cre-based transgenic reporter line [12,20]. ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer; ON, ON layer of the inner plexiform layer; OFF, OFF layer of the inner plexiform layer; 3V, third ventricle; SCN, suprachiasmatic nucleus; dLGN, dorsal lateral geniculate nucleus; IGL, intergeniculate leaflet; vLGN, ventral lateral geniculate nucleus. (Images courtesy of Steven Hughes.)

[9,10]. It appears that in addition to visual areas of the brain, including recently, studies have shown that a classical photoreceptor adaptation, the dLGN and superior colliculus small number of M1 ipRGCs (w7%) neural circuitry (network) adaptation in [11–14] (Figure 1), both of which have recurrent axon collaterals that both the retina and brain are critical to represent primary relay centres for terminate in the inner plexiform layer maximizing information coding from image-forming vision. It remains to [19], and on rare occasions ipRGC the visual world. Much of these be resolved if these innervations are projections can also be observed adaptations involve referencing the providing additional parallel signals for extending deeper into the retina photoreceptoral (rod/cone) signal to retinal luminance. It may be that the towards the outer plexiform layer the local luminance. However, in order primary influence is at the retinal level (Figure 1). At present the function to create efficient representations of and that the additional projections are of these retrograde connections is dynamic natural scenes it is often there to safeguard against the problem unknown, but it is clear that they necessary to adjust localised retinal known as ‘coding catastrophe’ [15], represent a potential mechanism for contrast circuits according to levels of so that downstream processes can transmitting irradiance information to luminance present across the visual be calibrated against levels of retinal the outer retina. field. At present, the mechanisms by adaptation in order to prevent It is now becoming increasingly clear which this is achieved are not well misinterpretation of the visual scene. that the function of melanopsin is not defined. It is now clear that melanopsin Interestingly, it has been suggested restricted to non-image forming function affects visual pathways, that dLGN projecting M4 type ipRGCs pathways, but instead melanopsin and the latest data suggest that may perform roles in contrast irradiance detection should now be melanopsin-expressing ipRGCs affect detection [13,16], although Allen et al., recognized as a key component of the visual coding at the level of the retina did not observe changes in contrast visual pathways of the mammalian and dLGN, most probably through local sensitivity of cone ERGs under mel-low retina. Based on recent data it seems retinal control of contrast and spatial conditions. now may be the time to re-evaluate processing. These data provide Secondly, it remains unclear by what our current models for luminance compelling evidence that signals from mechanism ipRGCs are able to interact channels in the primary visual pathway. melanopsin-expressing ipRGCs with the visual pathways of the retina. Currently we still know very little about provide a local measure of irradiance ipRGCs appear to communicate with sources or mechanisms encoding to regulate levels of light adaptation in other retinal neurones via gap junction background luminance at the highest the mammalian retina. connections [3]. There is also good level of the visual pathway. These There are, however, a series of evidence for retrograde signalling from findings also highlight the possibility questions that remain to be resolved. M1 type ipRGCs to dopaminergic that abnormalities in the function of Firstly, specific classes of melanopsin amacrine cells [17], which are well ipRGCs may represent another cells are now known to project placed to exert widespread influences potential source of clinical visual directly to important retino-recipient on retinal light responses [18]. More dysfunction in man. Dispatch R1057

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Behavioral Plasticity: A Nose for allows males to leave food patches depleted of mates and explore other Every Season territories in search of mates, thus increasing evolutionary fitness. Furthermore, the authors show that one A recent study in Caenorhabditis elegans identifies the dynamic expression of underlying molecular mechanism for a single odorant receptor as a molecular mechanism for context-dependent sex-specific differences in food modulation of olfactory preferences and food prioritization. attraction is the expression of a single olfactory receptor gene. Adult males Arantza Barrios behavioral prioritization in have reduced or absent expression Caenorhabditis elegans. of the diacetyl receptor ODR-10 in the In an ever-changing environment, Sexual reproduction in animals gender-shared chemosensory neuron animals need to reversibly and imposes differences in parental AWA. dynamically adapt their behavior investment including gamete But the findings of Ryan et al. do to meet their specific needs and production, mate choice and parental not end here. Behavioral priorities challenges in each context. In recent care. In C. elegans, too, priorities are not only different between sexes; years there has been a renewed are influenced by differences in priorities also change over time in interest in the mechanisms regulating reproductive needs. C. elegans males individuals. Surely, not many of us context-dependent modulation of must find mates (i.e., hermaphrodites) would choose to invest money on a behavior [1]. While the focus has been to reproduce, whereas retirement plan at 18, or throw money on the role of neuromodulators and hermaphrodites, which are essentially at the bar in a nightclub every Friday how they alter neural circuit properties sperm-carrying modified females, can night at 80. Similarly, C. elegans males to provide behavioral plasticity [2], reproduce by self-fertilization. do not always prioritize sex over food. less is known about the molecular Accordingly, the male devotes most Ryan et al. show that sexually immature effectors of behavioral decisions. In of his exploration to find a mate, males at the third larval (L3) stage this issue of Current Biology, Ryan et al. whereas the hermaphrodite explores chemotax towards food as efficiently [3] identify the dynamic expression mostly in search of food. as hermaphrodites and this too is of an odorant receptor as the common With a combination of cell-specific correlated with high levels of odr-10 molecular mechanism by which three genetic manipulations and cleverly expression in the AWA neurons of L3 dimensions of internal state — gender, designed behavioral assays, Ryan et al. males [3]. Previous experience is also developmental stage and nutritional [3] find that adult males chemotax an important determinant of priorities. status — regulate the olfactory less efficiently than hermaphrodites Starvation causes males to prioritize preferences linked to changes in towards food. Food desensitization food over sex [4,5], and this again is