ANIMAL BEHAVIOUR

Planning for breakfastSara J. Shettleworth

It is commonly believed that planning for the future is a skill unique to humans. Could other animals, even those as evolutionarily distant as western scrub-jays, share this skill with us?

Can it ever be said that animals plan ahead? Animals do show behaviour that prepares them for the future, but in general that behaviour reflects unlearned or conditioned responses to predictive cues. For example, a swallow fly-ing south or a marmot entering hibernation is reacting to a cue that has foretold the seasons for its ancestors. A hungry rat pressing a lever that provides food in ten seconds, rather than a lever providing food later, does so because rewards are more effective after short than after long delays. Two requirements1 for genuine future planning are that the behaviour involved should be a novel action, or combination of actions (thus ruling out migrating and hibernating), and that it should be appropriate to a motiva-tional state other than the one the animal is in at that moment (thus ruling out the rat’s lever pressing). In their report of two experiments with western scrub-jays (page 919 of this issue2), Raby et al. describe the first observations that unambiguously fulfil both requirements.

The scrub-jay (Fig. 1) naturally caches food. In Raby and colleagues’ research, jays were first allowed to acquire information about where food would be available in the morning. Then, in a test in the evening, the authors found that the birds behaved as if they were planning for breakfast by caching food items in the place where the food was most likely to be needed. The birds lived in large cages with three com-partments (rooms) (see Fig.1 of the paper on page 919). In the first experiment, each evening they ate powdered pine nuts, food they were unable to cache, in the central room. Then the next morning each bird was confined to one of the end rooms for two hours. In the ‘breakfast room’, a bird was always fed, whereas in the ‘no-breakfast room’ no food was given.

The test of planning came after several cycles of this treatment. For the first time, whole pine nuts were provided in the central room in the evening, along with sand-filled trays for cach-ing in the two end rooms. The authors found that the birds cached three times as many pine nuts in the no-breakfast room as in the break-fast room. Importantly, all the data came from this one test: learning how their choices deter-mined the next day’s breakfast could not have influenced the jays’ behaviour.

In the second experiment, the birds learned to expect breakfast in both rooms, peanuts only in one and dog kibble only in the other. On their first opportunity to cache peanuts and dog kibble in the evening, they distributed their caches so as to provide each room with the kind of food it usually lacked.

The results of two recent studies have been proposed as evidence for planning in pri-mates. In one3, monkeys chose between eating four dates and one date. Eating dates makes monkeys thirsty, and the animals received water after a shorter delay if they chose one date. They gradually reversed their natural preference for four dates as if taking account of future thirst. However, this study falls short of the demonstration with the western scrub-jays2 because the monkeys underwent repeated trials in which they learnt the consequences of their choices. In the other study4, bonobos and orangutans were taught to use a tool to obtain a treat and were then allowed to choose a tool

to take out of the testing room for use when they returned later. Most animals did take the appropriate tool on some trials. But in addi-tion to other problems5, individual animals’ patterns of success were far from consistent with a true understanding of the task.

Not much more than 100 years ago, inter-preting any of these observations as human-like planning would not have been problematic. Indeed, Darwin’s6 programme for document-ing evolutionary continuity between human minds and those of other species encouraged anthropomorphic interpretations of animal behaviour7. This attitude was largely replaced, in both experimental psychology7 and ethol-ogy8, by a bias against ‘mentalistic’ explana-tions. But recent years have seen a resurgence of attempts to document processes in animals that in humans are accompanied by distinc-tive conscious states. Besides thinking about the future, examples include awareness of other individuals’ states of mind, understanding how

Figure 1 | Food for thought. Raby and colleagues’ experiments2 with western scrub-jays show that these birds plan for the future by preferentially caching food where it will be needed most.

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tools work, intentional deception, and empa-thy. This trend has been impelled by several developments. These include Donald Griffin’s9 exhortations to ethologists to tackle animal consciousness; legitimization of the study of consciousness in the cognitive sciences gen-erally; and the prospect of understanding the neural and genetic bases of conscious processes using ‘animal models’. This last interest partly explains the current resurgence of attempts to study future planning in animals.

In humans, the ability to imagine future events and consciously recollect past ones (epi-sodic memory) is impaired in patients with damage to the region of the brain known as the hippocampus. Furthermore, new imaging stud-ies show that some of the same brain areas are active during both planning and remembering in normal adults10. Future planning and episodic memory are thus increasingly seen as part of a single human faculty for mental time travel, a faculty that other species have been proposed to lack1. Of course, as Raby and colleagues2 acknowledge, we will never know if a non-ver-bal animal is actually ‘mentally time travelling’ anywhere — future or past. Still, it is interesting that birds of the same species that show evi-dence of future planning also show episodic-

like memory11. In both cases, researchers have cleverly exploited scrub-jays’ specialized food caching to tackle questions of general interest in the study of cognitive evolution. But people can plan for, or think back on, much more than breakfast. It remains to be seen whether the abilities that scrub-jays show when caching are similarly applicable in other contexts. ■ Sara J. Shettleworth is in the Departments of Psychology and of Ecology and Evolutionary Biology, University of Toronto, Toronto M5S 3G3, Canada.e-mail: shettle@psych.utoronto.ca

1. Suddendorf, T. & Busby, J. Learn. Motiv. 36, 110–125 (2005).

2. Raby, C. R., Alexis, D. M., Dickinson, A. & Clayton, N. S. Nature 445, 919–921 (2007).

3. Naqshbandi, M. & Roberts, W. A. J. Comp. Psychol. 120, 345–357 (2006).

4. Mulcahy, N. J. & Call, J. Science 312, 1038–1040 (2006).5. Suddendorf, T. Science 312, 1006–1007 (2006).6. Darwin, C. The Descent of Man and Selection in Relation to

Sex (Murray, London, 1871).7. Boakes, R. From Darwin to Behaviourism (Cambridge Univ.

Press, 1984).8. Kruuk, H. Niko’s Nature (Oxford Univ. Press, 2003).9. Griffin, D. R. The Question of Animal Awareness (Rockefeller

Univ. Press, New York, 1976).10. Addis, D. R., Wong, A. T. & Schacter, D. L. Neuropsychologia

45, 1363–1377 (2007).11. Clayton, N. S. & Dickinson, A. Nature 395, 272–274 (1998).

ORGANIC CHEMISTRY

A tuxedo for iodine atomsPhil S. Baran and Thomas J. Maimone

Iodine atoms can be fitted with a chemical jacket to control the conversion of simple carbon chains into complex iodine-containing molecules. Previously, such reactions were only possible with enzymes.

The biosynthesis of hopene molecules show-cases a spectacular enzyme-catalysed reac-tion. In one fell swoop, a simple floppy chain of carbon atoms is transformed by a cyclase enzyme into a complex system containing molecular rings, arranged in a well-defined, three-dimensional shape1,2. This cyclization process creates five carbon–carbon bonds and nine stereogenic centres — asymmetric carbon atoms that are especially difficult to prepare in a controlled way. Furthermore, the reaction is enantioselective, meaning that only one of two possible mirror-image (chiral) forms of the molecule is produced. Chemists can only envy this exquisite level of molecular manipulation.

Amazingly, this type of reaction is not unique. It is just one of hundreds of similar naturally occurring transformations used to create the molecules of life. A common thread in these reactions is that a hydrogen atom is transferred from an enzyme to a specific loca-tion in the product (Fig. 1a). But other atoms may also be introduced enzymatically at this position, such as oxygen and, more exoti-cally, halogens — chlorine, bromine or iodine.

Although chemists have successfully emulated certain aspects of these cyclization reactions, the incorporation of halogen atoms has been a long-standing challenge. The first bromine-induced cyclization was observed more than 40 years ago3, but only as a side reaction and without any enantioselectivity. On page 900 of this issue, Ishihara and colleagues4 report a tremendous advance: the first non-enzymatic, high-yielding, enantioselective cyclization induced by a halogen atom.

In recent years, chemists have edged closer to recreating the power of enzymes in these reactions. Indeed, the challenge of cyclizing substrates using the equivalent of a chiral hydrogen ion (H+) — so mimicking the hopene biosynthesis — has already been met by Ishi-hara and Yamamoto’s group5, yielding products with a moderate excess of one chiral form over the other. They designed an artificial cyclase that delivers H+ to the substrate from one side only. The imitation enzyme was a sort of chem-ical tuxedo for H+ — a molecule that surrounds the ion, simulating the chiral environment found in natural cyclase. The whole assembly was activated by the addition of a Lewis acid

(a molecule that accepts electron pairs from other molecules) to dramatically increase the acidity and reactivity of the H+ ion.

So far, so good, but one objective still remained: to accomplish a so-called halo-cyclization. This is the same type of reaction as described above, but using a halogen atom rather than H+. Thousands of exotic halo-genated compounds have been isolated from natural sources, many of which show promise as medicinal leads for the treatment of vari-ous diseases. Several of these compounds have structures that probably arise from enzymatic reactions resembling the remarkable hopene cyclization, but initiated with a halogen atom6. For this reason, synthetic halocyclizations are highly desirable. But there are many inherent problems that must be solved to perform this reaction in the laboratory, which makes the present accomplishment by Ishihara and co-workers4 all the more impressive.

The authors required a highly reactive rea-gent that acts as a halogen source and that gives only one chiral product in a halocycli-zation reaction (Fig. 1b). They chose to work with iodine, and designed a reagent that is conceptually similar to the chiral H+ complex described above. The new reagent comprises a chemical tuxedo that fits around an iodine atom, creating a chiral environment for, and enhancing the reactivity of, that atom. Instead of using a Lewis acid to activate the assembly, the authors used a Lewis base (an electron-pair donor). The resulting ‘halocyclase’ is capable of converting simple hydrocarbons into iodinated architectures containing carbon rings, with near-enzyme-like control of the enantioselec-tivity. To explain this phenomenal selectivity, the authors suggest that the starting material and the iodine atom must square up to each other in just one optimal alignment before the reaction can proceed, in much the same way that two people must face each other before they can shake hands.

As with any breakthrough, there is still more work to be done. Although this halocyclization can also be initiated with bromine, the reaction is only enantioselective if iodine is used. The authors get around this problem by demon-strating that iodine atoms in the product can be transformed into other halogens without affecting the all-important chiral form of the product. Another limitation is that the reac-tion requires one molar equivalent of the chiral promoter — this is inefficient, as, in principle, a smaller quantity of the promoter should suf-fice. However, the authors have shown that other simple promoters can be used catalyti-cally, if not enantioselectively, thus opening the door for future advances in this area. Finally, more ‘halocyclases’ are necessary, as many of the halocyclizations reported in this work ter-minate after the first ring is formed, thereby requiring a second acid-catalysed step to forge the remaining rings.

Before this work, there were no halocycli-zation methods that approached the exquisite

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