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2. Helbing, D., Molnar, P., Farkas, I.J., andBolday, K. (2001). Self-organizing pedestrianmovement. Environment and Planning B:Planning and Design 28, 361–383.

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4. Schneirla, T.C. (1944). A unique case of circularmilling in ants, considered in relation to trailfollowing and the general problem oforientation. American Museum Novitates 1253,1–26.

5. Buhl, J., Sumpter, D.J., Couzin, I.D., Hale, J.J.,Despland, E., Miller, E.R., and Simpson, S.J.(2006). From disorder to order in marchinglocusts. Science 312, 1402–1406.

6. Parrish, J.K., Viscido, S.V., and Grunbaum, D.(2002). Self-organized fish schools: anexamination of emergent properties. Biol. Bull.202, 296–305.

7. Angelini, T.E., Hannezo, E., Trepat, X.,Marquez, M., Fredberg, J.J., and Weitz, D.A.(2011). Glass-like dynamics of collective cellmigration. Proc. Natl. Acad. Sci. USA 108,4714–4719.

8. Zhang, H.P., Be’er, A., Florin, E.L., andSwinney, H.L. (2010). Collective motion anddensity fluctuations in bacterial colonies. Proc.Natl. Acad. Sci. USA 107, 13626–13630.

9. Szabo, B., Szollosi, G.J., Gonci, B., Juranyi, Z.,Selmeczi, D., and Vicsek, T. (2006). Phasetransition in the collective migration of tissuecells: experiment and model. Phys. Rev. E Stat.Nonlin. Soft Matter Phys. 74, 061908.

10. Liu, L., Tuzel, E., and Ross, J.L. (2011). Loopformation of microtubules during gliding athigh density. J. Phys. Condens. Matter 23,374104.

11. Schaller, V., Weber, C., Semmrich, C., Frey, E.,and Bausch, A.R. (2010). Polar patterns ofdriven filaments. Nature 467, 73–77.

12. Lindemann, C.B., and Lesich, K.A. (2010).Flagellar and ciliary beating: the proven andthe possible. J. Cell Sci. 123, 519–528.

13. Dixit, R., and Cyr, R. (2004). Encountersbetween dynamic cortical microtubulespromote ordering of the cortical array throughangle-dependent modifications of microtubulebehavior. Plant Cell 16, 3274–3284.

14. Peterman, E.J., and Scholey, J.M. (2009).Mitotic microtubule crosslinkers: insights frommechanistic studies. Curr. Biol. 19,R1089–R1094.

Department of Bioengineering, 229 HallowellBuilding, Pennsylvania State University,University Park, PA 16802, USA.E-mail: wohbio@engr.psu.edu

DOI: 10.1016/j.cub.2012.04.045

Associative Learning: PavlovianConditioning without Awareness

Can Pavlovian conditioning occur outside of awareness? Yes, according toa new study showing that, under a particular set of circumstances, visualstimuli can become associated with aversive outcomes without participantsever seeing the stimuli.

Joel Pearson

There is an ongoing debate as to therole of conscious awareness inPavlovian conditioning. This process,in which neural representations ofevents correlated in the world becomelinked in the neural systemsrepresenting them, is often measuredbehaviourally by distinct physiologicalreflexes. Associative learning becamefamously linked to the work of IvanPavlov and his experiments onsalivation in dogs. Pavlov’s workinvolved ringing a bell right before thedogs were fed. He learnt that with timethe dogs would actually salivate inresponse to the sound of the bell alone,showing they had learned theassociation between the bell andthe food.

Despite forms of conditioning havingbeen demonstrated in a diverse rangeof organisms including the sea slugAplysia [1], the question as to the roleof awareness in this process oflearning has stirred up considerabledebate [2]. Studying consciousawareness in non-human animals thatcannot explicitly report theirphenomenological experience oftencomes with thorny philosophicalassumptions about interpretingbehaviour, so most work on the role

of awareness has involved humanparticipants. Until recently, much ofthis research has been hindered bymethodological constraints. A paper inthis issue of Current Biology by Raioet al. [3] reports perhaps the mostcompelling evidence to date thatPavlovian conditioning can arisewithout conscious awareness.

The authors utilised a relatively newtechnique developed for studyingvision and visual awareness called‘continuous flash suppression’ [4–6].Continuous flash suppression is moreor less a form of binocular rivalrypushed to its extreme. During binocularrivalry two dissimilar visual patterns arepresented, one to each eye, so theobserver’s brain is forced to try andreconcile these two very differentimages to exist at the one placesimultaneously. Rather than seeing onetransparent fused coherent stableimage, observers see something ofteninitially shocking — their visualawareness of the two patternsalternates back and forth over time, inno predictable manner. While eachpattern is presented to and processedby one eye and subsequent brainareas, an individual sees only one of thepatterns, while the other is suppressedoutside of awareness. This processprovides a valuable opportunity to

examine the extent of neuralprocessing and effects of visual stimulion behaviour without awareness.Forms of binocular rivalry have beenutilised to study many processes andphenomena outside of awareness,such as spatial orientation processing[7], motion perception [8], emotion [9],object processing [10] and even sexualorientation [11].Continuous flash suppression has

similar properties to binocular rivalry,but one of the images continuouslyflickers (at w10 Hz) between differentbrightly coloured patterns. Thesebright flashes (or coloured visualtransients) have the power to supressa stimulus in the other eye for extendedperiods, often for a few seconds.Continuous flash suppression is thusone of the most powerful methods forrendering a normal visual stimulusinvisible.Raio et al. [3] used continuous flash

suppression to render images of maleand female faces invisible or outside ofawareness. For half of these invisiblepresentations one set of faces, say themales, was immediately followed bya brief electrical shock to the wrist,while the female set was not. Randomlyinterleaved between these reinforcedtrials were non-reinforced test-trials ofboth male and female faces (stillvisually suppressed). The skinconductance response during thesetest-trials increased after only a fewpresentations of the training orconditioning trials. In other words, theassociative learning effect (greater skinconductance to the faces that werefollowed by a shock) occurred eventhough the subjects were never awareof the face stimuli during the

Current Biology Vol 22 No 12R496

conditioning or test trials. Furthermore,the authors had participants reportif they saw a face on each trial;in fact participants had to makea two-alternative forced-choicedecision whether the face was maleor female — participants’ decisionswere just below chance. After thisdiscrimination task participantshad to rate the confidence of theirchoice — confidence ratings wereno higher on correct trials thanincorrect trials.

The conditioning or learning effectsoutside of awareness reported byRaio et al. [3] display some distinctcharacteristics that differentiate themfrom learning with awareness. Thelearning effects appeared very rapidlyand subsequently diminished veryrapidly. Unlike normal learning theseeffects faded during furtherconditioning, whereas typically in thiskind of conditioning experiment thelearning would continue beforestabilising. Such brevity in associativelearning dynamics is clearly distinctfrom typical conditioning effects,which often last for days. Might thislearning outside of awareness betapping into a categorically differentlearning mechanism, or perhapsa subset of normal learning processes?This is an interesting idea that iscompatible with the data in the newstudy [3].

Raio et al. [3] did include a fully visiblecondition, which showed a verydifferent temporal learning profile. Intheir visible condition, however, boththe learning and test-trials were bothvisible, while in the unaware conditionboth the training and test-trials wereinvisible. Hence, we do not havea conscious measure of conditioningoutside of awareness, only anunconscious one. To help clarify theunderlying mechanism what is neededis a third condition in which only thetest trials are visible while the trainingtrials remain suppressed fromawareness. Such an experiment wouldhelp tease apart the nature of thisunconscious learning.

Previous claims of unconsciousconditioning have been criticised ona number of methodological groundssuch as trial sequence artifacts, failureto assess participant hypotheses, andinsensitivity to partial awareness [2]. Infact, some researchers have gone sofar as to argue that all conditioninginvolves cognitive representation andhence conscious awareness [12].

Others maintain that conditioning iscarried out by a separately evolvedspecialised system [13,14]. Willcontinuous flash suppression finallyprovide the experimental tool toresolve this long-standing debate?Watch this space!

Associative learning is thought toform the backbone of the mechanismsof many psychological disorders andtheir treatments [15,16]. Manybehavioural interventions forpsychological disorders rely oncounterconditioning or extinction-likeapproaches, such as cognitivebehavioural therapy. Does this newpaper by Raio et al. [3] shed light on anynew clinical treatment possibilities?Potentially yes, if mechanisms ofassociative learning can operatewithout awareness, it is possible toimagine a future non-intrusivetreatment option that might be run onpatients without their consciousinvolvement. However, the brief lifetimeof the effects in the new papermight limit any potential clinicalapplications.

References1. Carew, T.J., Walters, E.T., and Kandel, E.R.

(1981). Classical conditioning in a simplewithdrawal reflex in Aplysia californica. J.Neurosci. 1, 1426–1437.

2. Lovibond, P.F., and Shanks, D.R. (2002). Therole of awareness in Pavlovian conditioning:empirical evidence and theoreticalimplications. J. Exp. Psychol. Anim. Behav.Proc. 28, 3–26.

3. Raio, C., Carmel, D., Carrasco, M., andPhelps, E.A. (2012). Nonconscious fear isquickly acquired but swiftly forgotten. Curr.Biol. 22, R477–R479.

4. Tsuchiya, N., and Koch, C. (2005). Continuousflash suppression reduces negativeafterimages. Nat. Neurosci. 8, 1096–1101.

5. Tsuchiya, N., Koch, C., Gilroy, L.A., andBlake, R. (2006). Depth of interocularsuppression associated with continuous flashsuppression, flash suppression, and binocularrivalry. J. Vis.n 6, 1068–1078.

6. Stein, T., Hebart, M.N., and Sterzer, P. (2011).Breaking continuous flash suppression: a newmeasure of Uunconscious processing duringinterocular suppression? Front. Hum. Neurosci.5, 167.

7. Pearson, J., and Clifford, C.W. (2005).Suppressed patterns alter vision duringbinocular rivalry. Curr. Biol. 15, 2142–2148.

8. Blake, R., Tadin, D., Sobel, K.V., Raissian, T.A.,and Chong, S.C. (2006). Strength of early visualadaptation depends on visual awareness. Proc.Natl. Acad. Sci. USA 103, 4783–4788.

9. Pasley, B.N., Mayes, L.C., and Schultz, R.T.(2004). Subcortical discrimination ofunperceived objects during binocular rivalry.Neuron 42, 163–172.

10. Almeida, J., Mahon, B.Z., Nakayama, K., andCaramazza, A. (2008). Unconscious processingdissociates along categorical lines. Proc. Natl.Acad. Sci. USA 105, 15214–15218.

11. Jiang, Y., Costello, P., Fang, F., Huang, M., andHe, S. (2006). A gender- and sexualorientation-dependent spatial attentional effectof invisible images. Proc. Natl. Acad. Sci. USA103, 17048–17052.

12. Mitchell, C.J., De Houwer, J., andLovibond, P.F. (2009). The propositional natureof human associative learning. Behav. BrainSci. 32, 183–198, discussion 198–246.

13. Clark, R.E., and Squire, L.R. (1998). Classicalconditioning and brain systems: the role ofawareness. Science 280, 77–81.

14. Ohman, A., and Mineka, S. (2001). Fears,phobias, and preparedness: toward an evolvedmodule of fear and fear learning. Psychol. Rev.108, 483–522.

15. Rauch, S.L., Shin, L.M., and Phelps, E.A. (2006).Neurocircuitry models of posttraumatic stressdisorder and extinction: human neuroimagingresearch–past, present, and future. Biol. Psych.60, 376–382.

16. Milad, M.R., Rauch, S.L., Pitman, R.K., andQuirk, G.J. (2006). Fear extinction in rats:implications for human brain imaging andanxiety disorders. Biol. Psychol. 73, 61–71.

School of Psychology, The University ofNew South Wales, Sydney, Australia.E-mail: Joel@pearsonlab.org

DOI: 10.1016/j.cub.2012.04.042

Nuclear Positioning: Dynein Neededfor Microtubule Shrinkage-CoupledMovement

Nuclear movement often requires interactions between the cell cortex andmicrotubules. A new study has revealed a novel protein interaction linkingmicrotubule plus-ends with the cortex and a role for dynein in microtubuleshrinkage-coupled movement.

Xin Xiang

Proper positioning of nuclei andmitoticspindles is crucial for the normalgrowth and development of many

eukaryotic organisms [1]. Unlike othercellular organelles that move alongmicrotubule tracks, nuclei/spindlesmove in response to either pushingor pulling force on the microtubules