6. Olsen, K.H., Grahn, M., and Lohm, J.(2003). The influence of dominance anddiet on individual odours in MHCidentical juvenile Arctic charr siblings. J.Fish Biol. 63, 855–862.

7. Levin, S.A. (1992). The problem ofpattern and scale in ecology. Ecology 73,1943–1967.

8. Moss, C.J., and Poole, J.H. (1983).Relationships and social structure of

African elephants. In Primate SocialRelationships. R.A. Hinde, ed.(Sunderland, MA: Sinauer), pp. 315–325.

9. Cerling, T.E., Wittemyer, G., Rasmussen,H.B., Vollrath, F., Cerling, C.E., Robinson,T.J., and Douglas-Hamilton, I. (2006).Stable isotopes in elephant hairdocument migration patterns and dietchanges. Proc. Natl. Acad. Sci. USA 103,371–373.

Department of Zoology, University ofOxford, Oxford OX1 3PS, UK, andDepartment of Ecology andEvolutionary Biology, PrincetonUniversity, Princeton, New Jersey08544, USA.

DOI: 10.1016/j.cub.2006.02.042

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Time Perception: Space–Time inthe Brain

Accurate timing over the sub-second scale is essential for a range ofhuman perceptual and motor activities, but the mechanisms forencoding this time scale are poorly understood. Recent work issuggesting that timing does not involve a centralised clock, butpatterning within a distributed network.

David Burr1 andConcetta Morrone2

Time perception over fine scalesis fundamental to many aspects ofour lives, including speechrecognition and production,motion perception, soundlocalisation and fine motorcoordination. Many of these tasksdo not require explicit encoding oftime: perception of visual motion,for example, relies on the outputof spatio-temporally tunedneurons rather than onindependent estimates of spaceand time. However, the consciousawareness of the passage of timeand judgement of duration dorequire an explicit representationof time. Although we now have aquite firm understanding of themechanisms of many processesthat involve temporal encoding —such as binaural soundlocalisation and motionperception — the mechanismsthat allow us to estimate theduration of events are far moreelusive.

The prevailing model for eventtiming has involved a centralisedinternal clock or pacemakerfeeding into an accumulator (forexample, see [1,2]). More recentmodels, however, considerdistributed timing networks, withdifferent mechanisms timingdifferent interval lengths [3,4].While there is good evidence fordifferent clocks for differentinterval lengths, most evidence to

date suggests that clockstranscend sensory modalities. Forexample, performance in rhythmictapping is well correlated with theability to judge the length ofauditory intervals of similarperiodicity [5], implying a commonmechanism. Similarly, training insomatosensory intervaldiscrimination — which can causea 2-fold improvement inperformance — generalisesacross skin locations and alsoacross modalities to improveauditory discrimination of similarintervals [6], and learning a visualdiscrimination of stimuli presentedto the left visual hemifieldtransfers completely to stimuli inthe right hemifield [7].

A new study, reported in thisissue of Current Biology,questions the notion ofcentralised cross-modal clocks.Johnston et al. [8] have shown

that adaptation to a fast-moving(20 Hz) spatially localised gratingdecreases the apparent durationof subsequently presentedgratings by about 17% (Figure 1).The adaptation does not affect theapparent duration of auditorytones, nor of visual stimulidisplayed to spatially differentpositions, whether in the same ordifferent hemifield. Various controlexperiments excluded thepossibility that apparent temporalfrequency, reduced viaadaptation, was responsible forthe diminution in apparentduration. Interestingly, theadaptation did not affect theperceived onset or offset of thevisual stimuli (measured byauditory matching), only theapparent duration between them.

The results suggest that thetiming of visual events is morecomplicated than counting thepulses of a centralisedpacemaker: not only wereauditory events unaltered, but theadaptation was spatially specific.Johnston et al. [8] argue that theirresults show that duration isgoverned by a spatially localisedtemporal rate signal that issubject to adaptation; this wouldbe consistent with classical andrecent work showing that moving

Figure 1. The main experimentof Johnston et al. [8].

Subjects fixed at centre whileobserving a spatially localisedgrating move rapidly, alter-nately leftwards and rightwards,for 15 s. After a brief pause a‘standard’ grating was pre-sented for 600 ms on theunadapted side (brownsymbols) followed (or pre-ceded) by a probe of variableduration on the adapted side(grey symbols), and subjectsasked to judge which appearedlonger (in the actual experimentthey were sequential not simultaneous). In order to appear the same duration as the stan-dard (brown bar), the probe presented to the adapted retina had to be about 100 ms(17%) shorter (grey bar).

15 s

0.6 s0.6 s

0.5 s

Perceived time

Current Biology

Current Biology Vol 16 No 5R172

Figure 2. An artist’s impression of the intrinsic connections of space and time, and howrelativistic-like effects could compress perceptual space and time.

targets appear to last longer thanstationary targets [9,10]. Theyfurther speculate that the purposeof the adaptation might be tomaintain temporal calibration overspace: as the temporal statisticsof natural scenes tend to bespatially invariant, localadaptation provides an effectivecalibration strategy.

While the results certainly pointto decentralised timing control, itis hard to imagine how theadaptation might serve afunctionally useful role in‘calibrating’ time across space.The temporal statistics of ourretinae are in fact rarelyhomogeneous: simply walkingthrough the environment createsa complex optic-flow pattern,with the point of headingessentially stationary while thescenery either side of the headingpoint streams rapidly by. Indeedlocal adaptation could be apotential problem, were theeffects not so small, around 17%,below the limit of temporaldiscrimination for these intervals(usually about 20% [7,8]).

A possible mechanism for theadaptation, briefly entertained byJohnston et al. [8], is that severalsystems are involved with eventtiming, such as the parvocellularand magnocellular systems that

are believed to carry differenttypes of visual information, andthat adaptation of one of thesedisrupts the balance betweenthem. Certainly this is a testableprediction, as various techniquesexist to isolate magnocellular andparvocellular function.

It is tempting to compare thisnew study with our own group’srecent work, which also arguesagainst centralised clocks. Wehave recently shown thatsaccadic eye movements cause adramatic, 2-fold reduction inapparent duration of visual, butnot auditory events [11](paralleling the spatialcompression that also occursduring saccades [12]). As themagnocellular system isselectively suppressed duringsaccades [13], it is possible thatthe two sets of results couldreflect some common cause. Butthere are some major differencesbetween the results. The effectsof saccades on duration that weobserved were much larger thanthose reported by Johnston et al.[8] and, under some conditions,they resulted in a reversal ofperceived order. Furthermore,saccades not only reducedapparent duration, but alsoincreased the precision of intervaljudgement commensurably,

preserving the Weber lawrelationship that characterisesinterval judgements [2,7]; whereasin Johnston et al.’s study [8]precision remained constantdespite the 17% reduction inperceived duration. While itremains to be seen how muchcommon ground may explain thetwo experiments, both pointclearly to the existence of visuallybased timing mechanisms.

It would be interesting to askwhether the spatial specificity isretinotopic or spatiotopic: that is,if the observer’s gaze changesbetween the adaptation and teststimuli, is the reduction inapparent duration specific to thepart of the retina that wasadapted or to the region ofexternal space? The answer tothis question could help to locatethe locus of the effect [14]. If thespecificity were retinotopic — if itfollows the eyes — it would pointto a fairly early stage of visualprocessing where receptive fieldsare locked to the retina, forexample, the magnocellularsystem of the thalamus and itstargets in V1 and V2. On the otherhand, if the adaptation werespatiotopic — fixed in externalcoordinates — it would implicatehigher levels of processing, suchas LIP, a visual area wherereceptive fields of cells move witheach eye movement. This wouldbe particularly exciting, as recentwell-controlled single-cell studieson awake monkeys have firmlyimplicated that area in timing theduration of visual events [15,16].

Whatever the mechanismsinvolved in the adaptation effects,these and other results [8,11]show that judging time is nosimple task for the brain.Centralised cross-modal clockscannot account for the newresults, but nor can their existencebe completely excluded, given thecross-modal correlation andlearning in duration discrimination[5,6]. However, the new results fitwell with recent thinking thatsuggests that, at least for shortintervals, time may not beencoded explicitly as a metric, butas a spatio-temporal pattern withina distributed network of neurons[17,18]. Relative time betweenevents may be transformed into

Dispatch R173

specific patterning in neural maps,interpretable with the same type ofmachinery used to decode corticalrepresentation of spatial images.

Much previous work ondynamic perception has shownthat for the brain time and spaceare not processed separately, butcan influence each other strongly[19]. The new study [8] points toanother example of the interactionbetween the two dimensions,showing that time analysis candepend on spatial position.Einstein’s stunning insight thatrevolutionised physics a centuryago was that space and time arein some sense ‘the same stuff’and can be treated in the sameway. Perhaps a similar conceptualleap is needed to understandspace-time in the brain. While thisline of thinking is clearly highlyspeculative, we have suggestedthat the effects of saccades ontemporal judgements may be arelativistic-like consequence ofrapidly shifting receptive-fields atthe time of saccades, that alsocause spatial compression [20](schematically illustrated in Figure2). It remains to be seen whetherthis approach will provide a usefulframework to study spatial andtemporal neural events.

Kerrie M. Swadling

Many small pelagic animalsundertake extensive daily verticalmigrations, sometimes travellinghundreds of meters to and fromthe food-rich surface layers of theocean. The classic paradigm hasorganisms ascending to the upperlayers at night to feed andreturning to deeper waters duringthe day to avoid visual predators,predominantly fish. It has longbeen assumed that they makeonly one round trip every 24 hr [1].

Krill Migration: UNight

A new study showing Antarctic krilhas provided indirect evidence thamigrations. Such behavior could mcarbon sequestration by the deep

References1. Treisman, M. (1963). Temporal

discrimination and the indifferenceinterval. Implications for a model of the‘internal clock’. Psychol. Monogr. 77,1–31.

2. Gibbon, J. (1977). Scalar expectancytheory and Weber’s Law in animaltiming. Psychol. Rev. 84, 279–325.

3. Buonomano, D.V., and Karmarkar, U.R.(2002). How do we tell time?Neuroscientist 8, 42–51.

4. Buhusi, C.V., and Meck, W.H. (2005).What makes us tick? Functional andneural mechanisms of interval timing.Nat. Rev. Neurosci. 6, 755–765.

5. Keele, S.W., Pokorny, R.A., Corcos,D.M., and Ivry, R. (1985). Do perceptionand motor production share commontiming mechanisms: a correctionalanalysis. Acta Psychol. (Amst.) 60,173–191.

6. Nagarajan, S.S., Blake, D.T., Wright,B.A., Byl, N., and Merzenich, M.M.(1998). Practice-related improvements insomatosensory interval discriminationare temporally specific but generalizeacross skin location, hemisphere, andmodality. J. Neurosci. 18, 1559–1570.

7. Westheimer, G. (1999). Discrimination ofshort time intervals by the humanobserver. Exp. Brain Res. 129, 121–126.

8. Johnston, A., Arnold, D.H., and Nishida,S. (2006). Spatially localised distortionsin event time. Curr. Biol., this issue.

9. Roelofs, C.O.Z. (1951). Influence ofdifferent sequences of optical stimuli onthe duration of a given interval of time.Acta Psychol. (Amst.) 8, 89–128.

10. Verstraten, F.A.J., Kanai, R.,Hogendoorn, J.H.A., and Paffen, C.L.E.(2005). Visual motion expands perceivedtime. Perception 34 (sup), 111.

11. Morrone, M.C., Ross, J., and Burr, D.(2005). Saccadic eye movements causecompression of time as well as space.Nat. Neurosci. 8, 950–954.

12. Ross, J., Morrone, M.C., and Burr, D.C.

While the vertical migration ofpopulations can be monitored bysampling with nets and otherdevices, uncovering themovements of individuals hasbeen more problematic. Indirectevidence — analysis of gutcontents — has suggested thatanimals move in and out of thefeeding zone, as individualscollected from deep waters atnight often contain prey that areonly present in surface waters [2].Direct verification of this,however, has been lacking. A new

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l sink when their stomachs are fullt krill undergo multiple daily verticalake a significant contribution tooceans.

(1997). Compression of visual spacebefore saccades. Nature 384, 598–601.

13. Burr, D.C., Morrone, M.C., and Ross, J.(1994). Selective suppression of themagnocellular visual pathway duringsaccadic eye movements. Nature 371,511–513.

14. Melcher, D. (2005). Spatiotopic transferof visual-form adaptation acrosssaccadic eye movements. Curr. Biol. 15,1745–1748.

15. Leon, M.I., and Shadlen, M.N. (2003).Representation of time by neurons in theposterior parietal cortex of the macaque.Neuron 38, 317–327.

16. Janssen, P., and Shadlen, M.N. (2005). Arepresentation of the hazard rate ofelapsed time in macaque area LIP. Nat.Neurosci. 8, 234–241.

17. Buonomano, D.V., and Merzenich, M.M.(1995). Temporal informationtransformed into a spatial code by aneural network with realistic properties.Science 267, 1028–1030.

18. Eagleman, D.M., Tse, P.U., Buonomano,D., Janssen, P., Nobre, A.C., andHolcombe, A.O. (2005). Time and thebrain: how subjective time relates toneural time. J. Neurosci. 25,10369–10371.

19. Burr, D.C. (2000). Motion vision: are‘speed lines’ used in human visualmotion? Curr. Biol. 10, R440–R443.

20. Morrone, M.C., Ross, J., and Burr, D.C.(2006). Keeping vision stable: rapidupdating of spatiotopic receptive fieldsmay cause relativistic-like effects. InProblems of Space and Time inPerception and Action, R. Nijhawan, ed.(Cambridge: CUP).

1Department of Psychology, Universityof Florence, Italy. 2Faculty ofPsychology, San Raffaele University,Milan, Italy.

DOI: 10.1016/j.cub.2006.02.038

study [3] has provided tantalisingevidence that one of the mostnumerically and ecologicallyimportant small pelagic species,Antarctic krill (Euphausia superba,Figure 1), undertake more thanone vertical migration per day. Asthey reported recently in CurrentBiology, by examining theswimming behavior of tetheredkrill, Tarling and Johnson [3] haveshown that individuals activelyreposition themselves lower in thewater column when theirstomachs are full.

Antarctic krill are negativelybuoyant and so must swimcontinuously to remain in thesurface layers; if they stopswimming, they sink. Fortunatelythey can exert some control overtheir rate of descent by adopting aparachute mode, in which they fanout their swimming legs and opentheir feeding baskets, to decrease