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Dispatches apply to the base of the animal tree of life. Instead, placozoans and cnidarians are probably simpler than some of their ancestors (i.e., the common ancestor they shared with ctenophores). This should actually not come as a surprise following the description of many independent cases of extreme simplification in parasitic metazoans, as exemplified by orthonectids [13] and myxozoans [14]. Ctenophores and their troubled phylogenetic position may hold the key to resolving some of these recalcitrant mysteries. REFERENCES
3. Nielsen, C. (1995). Animal Evolution, Interrelationships of the Living Phyla, 1st Edition (Oxford: Oxford University Press). 4. Dunn, C.W., Hejnol, A., Matus, D.Q., Pang, K., Browne, W.E., Smith, S.A., Seaver, E., Rouse, G.W., Obst, M., Edgecombe, G.D., et al. (2008). Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749. 5. Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G.W., Edgecombe, G.D., Martinez, P., Bagun˜a`, J., Bailly, X., Jondelius, U., et al. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B Biol. Sci. 276, 4261–4270. 6. Moroz, L.L., Kocot, K.M., Citarella, M.R., Dosung, S., Norekian, T.P., Povolotskaya, I.S., Grigorenko, A.P., Dailey, C., Berezikov, E., Buckley, K.M., et al. (2014). The ctenophore genome and the evolutionary origins of neural systems. Nature 510, 109–114.
1. Presnell, J.S., Vandepas, L.E., Warren, K.J., Swalla, B.J., Amemiya, C.T., and Browne, W.E. (2016). The presence of a functionally tripartite through-gut in ctenophora has implications for metazoan character trait evolution. Curr. Biol. 26, 2814–2820.
7. Whelan, N.V., Kocot, K.M., Moroz, L.L., and Halanych, K.M. (2015). Error, signal, and the placement of Ctenophora sister to all other animals. Proc. Natl. Acad. Sci. USA 112, 5773– 5778.
2. Agassiz, L. (1850). Contributions to the natural history of the Acalephæ of North America. Part II: On the beroid medusæ of the shores of Massachusetts, in their perfect state of development. Memoirs of the American Academy of Arts and Sciences. New Series 4, 313–374.
8. Ryan, J.F., Pang, K., Schnitzler, C.E., Nguyen, A.D., Moreland, R.T., Simmons, D.K., Koch, B.J., Francis, W.R., Havlak, P., Smith, S.A., et al. (2013). The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342, 1242592.
9. Pisani, D., Pett, W., Dohrmann, M., Feuda, R., Rota-Stabelli, O., Philippe, H., Lartillot, N., and Wo¨rheide, G. (2015). Genomic data do not support comb jellies as the sister group to all other animals. Proc. Natl. Acad. Sci. USA 112, 15402–15407. 10. Nosenko, T., Schreiber, F., Adamska, M., Adamski, M., Eitel, M., Hammel, J., Maldonado, M., Mu¨ller, W.E., Nickel, M., Schierwater, B., et al. (2013). Deep metazoan phylogeny: When different genes tell different stories. Mol. Phylogenet. Evol. 67, 223–233. 11. Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Que´innec, E., et al. (2009). Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 1–17. 12. Telford, M.J., and Copley, R.R. (2016). Zoology: War of the worms. Curr. Biol. 26, R335–337. 13. Mikhailov, Kirill V., Slyusarev, Georgy S., Nikitin, Mikhail A., Logacheva, Maria D., Penin, Aleksey A., Aleoshin, Vladimir V., and Panchin, Yuri V. (2016). The genome of Intoshia linei affirms orthonectids as highly simplified spiralians. Curr. Biol. 26, 1768– 1774. 14. Okamura, B., and Gruhl, A. (2016). Myxozoa + Polypodium: A common route to endoparasitism. Trends Parasitol. 32, 268–271.
Episodic Memory: Rats Master Multiple Memories William A. Roberts Department of Psychology, Western University, London, Ontario N6A 5C2, Canada Correspondence:
[email protected] http://dx.doi.org/10.1016/j.cub.2016.08.042
A new study in which rats had to discriminate odors according to whether they were novel for a particular environmental context has found that they can accurately discriminate a large number of odors and multiple context transitions, suggesting that they are able to form and remember multiple episodic memories.
People show phenomenal memory for pictures: when shown a list of over 2000 pictures, each briefly exposed, people accurately recognize seen pictures from unseen pictures with over 90% accuracy on a subsequent test [1]. Such an ability is undoubtedly underlain by a primate visual system highly developed for the recording and storage of visual images. If a person is exposed to a sequence of facial images of other people, some
images will seem familiar because they were first seen earlier in the list, and more recently seen faces will seem more familiar. The presentation of an historical figure, say Abraham Lincoln, will retrieve semantic or reference memories of general information about slavery and the American civil war. Still another picture in the sequence might be that of a close friend: this image retrieves multiple episodic memories of shared experiences
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that occurred at different times and in different contexts. In this issue of Current Biology, Panoz-Brown et al. [2] report that rats too can remember multiple episodic memories encoded in different contexts. It is widely acknowledged that animals form semantic memories, as they learn to make Pavlovian responses to conditioned stimuli or to make instrumental responses of lever pressing
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Dispatches or maze running for food reward. The question of whether animals form episodic memories of individual past experiences has been more controversial, with some suggesting that only humans are capable of episodic memory [3,4]. But there is mounting evidence that other animals can also remember separate past episodes. The key to this research has been the demonstration that animals remember different past events when exposed to different episodic cues associated with those events. Recent experimental tests have demonstrated ‘what-where-when’ memory in rats [5,6] and in several species of birds [7,8]. Thus, rats learn to return to the location (where) of a favored reward (what) after a specific time interval (when) has elapsed since first encountering the reward [5]. Similarly, scrub jays preferentially visit worm locations 4 hours after caching the worms, but preferentially visit cached peanuts 5 days later, after the worms have decayed [7]. As in the case of human episodic memory, time in the past when an event occurred is an important component of animal episodic memory. Another important cue used to retrieve episodic memories is the environmental context in which the memory was stored. In experiments studying memory for what-where-which (context), rats were allowed to explore two E-shaped arenas that differed in brightness and texture. Two novel objects (A and B) were both hidden in the end arms of the arenas, such that A was on the left and B was on the right in a black-smooth context, and B was on the left and A was on the right in a white-rough context. Rats were then tested by habituating them to object A or object B in a neutral setting and then allowing them to search for objects in each context. Given rats’ preference for novelty, they searched at the A location in both contexts after being habituated to B, and searched in the B location in both contexts after being habituated to A [9]. Choice of the location of the novel object was accomplished through episodic memory for the objects (what) and their locations (where) within each arena context (which).
In their new study, Panoz-Brown et al. [2] searched for another property of human episodic memory, the ability to store multiple episodic memories and the contexts in which they were formed. They took advantage of another recent discovery in the field of rodent memory: just as humans can remember a vast number of briefly seen visual images [1], rats can remember a large number of recently experienced odors [10]. After experiencing up to 70 or more different odors, rats chose between a novel odor and one previously experienced, with only choice of the novel odor rewarded (odor-span task). Rats chose the correct novel odor, thus rejecting the familiar remembered odor, on over 80% of the tests. A large olfactory bulb with multiple connections to the forebrain and brainstem in rats [11] underlies their high retention on the odorspan task. Panoz-Brown et al. [2] converted the odor-span task to an episodic memory test by testing rats’ memory for the same odors in different contexts. Two walled context arenas were used, both circular, with one twice the diameter of the other. The larger arena was white and contained 18 holes arranged in two concentric circles. The smaller arena had alternating black and white circles on its floor and contained eight holes along the wall, spaced equidistant apart. In these arenas, rats chose between two covered cups placed in two randomly chosen holes. There were 40 different lids that could be placed on these cups, with each lid containing a different odor. The odors used were commercially available scents or spices, such as cinnamon, lavender, or vanilla. All tests of episodic memory were carried out using both contexts. In an initial experiment, rats were tested in the order Context A/Context B/Context A, with the arena contexts counterbalanced. In their initial trials on Context A, they were exposed to eight different odors by giving them successive choices between a previously experienced odor and a new odor, with choice of the lid containing the new odor rewarded by a piece of chocolate in the cup beneath it (Figure 1). When switched to Context B, rats received 16 more choice trials, with eight new odors introduced. In Context B, rats then
Figure 1. A rat choosing between two containers covered with differently scented lids. The image shows a rat in a test arena choosing between two cups covered with lids saturated with different odors. The odor of one lid was previously experienced in the arena context shown, but the odor of the other lid had only been experienced in a larger arena with two concentric rings of cups. Rats significantly preferred the lid containing the odor novel to the test context and were rewarded with chocolate for making the correct choice. This finding shows that rats formed odor-context episodic memories. (Image courtesy Jon Crystal.)
encountered trials in which they experienced an odor previously chosen in Context A and a new odor not previously experienced in the session. The critical test came when rats were switched back to Context A and presented with a choice between an odor previously experienced in Contexts A and B and an odor experienced only in Context B. Although both odors were familiar from recent experience, rats chose the odor recently experienced in Context B on 75% of the trials, quite significantly above chance. Thus, if a rat sniffed a banana odor on a lid in Context A, and then sniffed banana again on a lid in Context B and strawberry for the first time on a lid in Context B, when given a choice between banana and strawberry lids in Context A, it significantly preferred the strawberry lid. How does this observation demonstrate episodic memory? The argument from this finding is that rats would only show a preference for strawberry because it is novel to Context A, whereas memory of banana in Context A is a familiar episodic memory. Various controls run in this experiment ruled out the possibility that choice of the odor novel to Context A was based on a difference in relative familiarity. In a subsequent experiment, rats were tested with five transitions between Contexts A and B. Thus, on some tests, an odor
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Dispatches experienced in Context B was tested against a correct odor experienced in Context A but novel to Context B. Rats continued to choose the correct odor on over 80% of the test trials. When carried to the extreme of 15 context transitions, with the point of transition unpredictable, rats continued to accurately choose the correct odor. A final experiment showed no loss of accuracy when a 45-minute retention interval was introduced between exposure to odors in contexts and the memory test. The scope of our knowledge about episodic memory in animals has expanded. Beyond demonstrations of memory for episodes retrieved by time and context, this new research shows us that animals (rats) can remember a large number of episodic memories when the same event (odor) is experienced in different contexts.
REFERENCES 1. Standing, L., Conezio, J., and Haber, R.N. (1970). Perception and memory for pictures: Single-trial learning of 2500 visual stimul. Psychonom. Sci. 19, 73–74. 2. Panoz-Brown, D., Corbin, H.E., Dalecki, S.J., Gentry, M., Brotheridge, S., Sluka, C.M., Wu, J.-E., and Crystal, J.D. (2016). Rats remember items in context using episodic memory. Curr. Biol. 26, 2821–2826. 3. Tulving, E. (2005). Episodic memory and autonoesis: uniquely human. In The Missing Link in Cognition: Origins of Self-Reflective Consciousness, H. Terrace, and J. Metcalfe, eds. (New York: Oxford University Press), pp. 3–56.
6. Zhou, W., and Crystal, J.D. (2011). Evidence for remembering when events occurred in a rodent model of episodic memory. Proc. Natl. Acad. Sci. USA 106, 9525–9529. 7. Clayton, N.S., and Dickinson, A. (1988). What, where, and when: Episodic-like memory during cache recovery by scrub jays. Nature 395, 272–274. 8. Feeney, M.C., Roberts, W.A., and Sherry, D.F. (2009). Memory for what, where, and when in the black-capped chickadee (Poecile atricapillus). Anim. Cog. 12, 767–777. 9. Eacott, M.J., and Easton, A. (2007). On familiarity and recall of events by rats. Hippocampus 17, 890–897.
4. Suddendorf, T., and Corballis, M.C. (2005). The evolution of foresight: What is mental time travel and is it unique to humans? Behav. Brain Sci. 30, 299–313.
10. April, L.B., Bruce, K., and Galizio, M. (2013). The magic number 70 (plus or minus 20): Variables determining performance in the rodent odor span task. Learn. Mot. 44, 143–158.
5. Babb, S.J., and Crystal, J.D. (2006). Episodiclike memory in the rat. Curr. Biol. 16, 1317– 1321.
11. Slotnick, B.M., and Schoonover, F.W. (1992). Olfactory pathways and the sense of smell. Neurosci. Biobehav. Rev. 16, 453–472.
Palaeontology: A Hook to the Past Nicholas C. Fraser National Museums Scotland, Chambers Street, Edinburgh EH1 1JF, UK Correspondence:
[email protected] http://dx.doi.org/10.1016/j.cub.2016.07.053
The poorly understood Triassic reptile Drepanosaurus is known for its excessively large claws. New discoveries demonstrate a remarkable modification of the bones in the wrist and forearm, a significant departure from the typical five-digit tetrapod limb. The limbs of most tetrapods have five fingers or toes. Apparently, it has been so since the first invasion of land by tetrapods 360 million years ago, and even today highly modified forelimbs, such as the wing of a bat or the flipper of a whale, essentially always comprise two elements, the radius and ulna, which run parallel to each other. Moreover, although the hand has been subject to much greater modification, in each instance it is relatively straightforward to establish how the basic structure of the five digits has been altered. Sometimes there is reduction or even loss of some digits, as in the hands and feet of perissodactyls, such as horses, or the feet of the meat-eating theropod
dinosaurs. In other instances, hypertrophy of digits and individual phalanges occurs, as in the pterosaur wing finger or the elongate fourth finger of the aye-aye’s hand. However, a new paper by Adam Pritchard and colleagues in this issue of Current Biology [1] describes a new fossil from approximately 220 million-year-old deposits in North America that challenges this conservative basic plan. Enter Drepanosaurus: this bizarre fossil was originally described on the basis of a single skeleton from northern Italy that is a bit reminiscent of a road-kill (Figure 1) [2,3]. Although it lacks a head, much of the rest of the body is preserved intact, including a very prominent tail,
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articulating hindlimbs and a bit of a crumpled ribcage. In front of the ribs, it starts to become a bit messy, and originally the forelimbs were considered to be at least partially disarticulated. Still, the animal was reconstructed in relatively conventional terms with broad and robust clavicles and interclavicle, a plate-like coracoid, and slender radius and ulna in the forelimb. However, the most striking feature of Drepanosaurus is an enormous hatchetshaped claw on the second digit of each hand, which marked this out as a very unusual animal (Figure 1). Now, Pritchard and colleagues [1] describe new Drepanosaurus material originating a few thousand miles away from the original
