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competition over who shall reproduce,but because it is apparently moreefficient for the colony to cyclebetween phases of reproduction andforaging. Why cycling should bemore efficient than continuousreproduction, as is seen in mosteusocial insects, has not yet beenaddressed. Perhaps it is the only waythese ants can control egg production.Interestingly, females of some solitaryinsects show similar cycling, and someaspects of the behaviour of eusocialspecies may be derived from thesecycles [9].

The Teseo paper [2] is importantbecause it brings into sharp focus therelative importance of colony conflictand colony efficiency in the evolution ofworker policing. In all other studysystems, conflict and efficiency areconfounded. A honey bee colony isless efficient if the workers lay eggs[10,11], but did policing first evolve toreduce genetic conflict or increasecolony-level efficiency? Teseo et al. [2]have demonstrated that efficiencyalone seems to maintain policing inC. biroi, but it still seems that in mostother cases it is kin conflict that hasdriven the evolution of worker policing.Predictions about policing behaviourfrom conflict theory are stronglysupported empirically [1,12]. So, itseems that both conflict and efficiencycan be important to the evolution ofpolicing. It is interesting to speculateon whether the policing behaviour

observed in C. biroi originally evolvedto resolve genetic conflict, and wasthen co-opted to its present function,or if it arose when the species becameclonal, abandoned queens andadopted its current practise ofreproductive cycling. In any case, itis now timely to re-emphasise thatthe concept of worker policingencompasses behaviour that improvescolony efficiency as well as resolvingconflict [13].

References1. Ratnieks, F.L.W., Foster, K.R., and

Wenseleers, T. (2006). Conflict resolution ininsect societies. Annu. Rev. Ent. 51,581–608.

2. Teseo, S., Kronauer, D.J.C., Jaisson, P., andChaline, N. (2013). Enforcement of reproductivesynchrony via policing in a clonal ant. Curr.Biol. 23, 328–332.

3. van Zweden, J.S., Cardoen, D., andWenseleers, T. (2012). Social evolution: Whenpromiscuity breeds cooperation. Curr. Biol. 22,R922.

4. Palmer, K.A., and Oldroyd, B.P. (2000).Evolution of multiple mating in the genus Apis.Apidologie 31, 235–248.

5. Ratnieks, F.L.W. (1988). Reproductiveharmony via mutual policing by workersin eusocial. Hymenoptera. Am. Nat. 132,217–236.

6. Ratnieks, F.L.W., and Visscher, P.K. (1989).Worker policing in honeybees. Nature 342,796–797.

7. Davies, N.B., Krebs, C.J., and West, S.A. (2012).An Introduction to Behavioural Ecology, 4thEdition (Chichester: Wiley-Blackwell).

8. Ravary, F., and Jaisson, P. (2002). Thereproductive cycle of thelytokous colonies ofCerapachys biroi Forel (Formicidae,Cerapachyinae). Ins. Soc. 49, 114–119.

9. Amdam, G.V., Csondes, A., Fondrk, M.K., andPage, R.E. (2006). Complex social behaviourderived from maternal reproductive traits.Nature 439, 76–78.

10. Montague, C.E., and Oldroyd, B.P. (1998). Theevolution of worker sterility in honey bees: aninvestigation into a behavioral mutant causinga failure of worker policing. Evolution 52,1408–1415.

11. Barron, A.B., Oldroyd, B.P., andRatnieks, F.L.W. (2001). Worker reproductionin honey-bees (Apis) and the anarchicsyndrome: A review. Behav. Ecol. Sociobiol.50, 199–208.

12. Wenseleers, T., Badcock, N.S., Erven, K.,Tofilski, A., Nascimento, F.S., Hart, A.G.,Burke, T.A., Archer, M.E., and Ratnieks, F.L.W.(2005). A test of worker policing theory in anadvanced eusocial wasp, Vespula rufa.Evolution 59, 1306–1314.

13. Zanette, L.R.S., Miller, S.D.L., Faria, C.M.A.,Almond, E.J., Huggins, T.J., Jordan, W.C., andBourke, A.F.G. (2012). Reproductive conflict inbumblebees and the evolution of workerpolicing. Evolution 66, 3765–3777.

14. Wenseleers, T., Tofilski, A., andRatnieks, F.L.W. (2005). Queen and workerpolicing in the tree wasp Dolichovespulasylvestris. Behav. Ecol. Sociobiol. 58,80–86.

15. Monnin, T., Ratnieks, F.L.W., Jones, G.R., andBeard, R. (2002). Pretender punishmentinduced by chemical signalling in a queenlessant. Nature 419, 61–65.

16. Pirk, C.W.W., Neumann, P., Hepburn, H.R.,Moritz, R.F.A., and Tautz, J. (2004). Egg viabilityand worker policing in honey bees. Proc. Nat.Acad. Sci. USA 101, 8649–8651.

17. Beekman, M., and Oldroyd, B.P. (2005). Honeybee workers use cues other than egg viabilityfor policing. Biol. Lett. 1, 129–132.

18. Wenseleers, T., Hart, A.G., and Ratnieks, F.L.W.(2004). When resistance is useless: Policingand the evolution of reproductive acquiescencein insect societies. Am. Nat. 164,E154–E167.

Behaviour and Genetics of Social InsectsLab, School of Biological Sciences A12,University of Sydney, Sydney, NSW 2006,Australia.E-mail: benjamin.oldroyd@sydney.edu.au

http://dx.doi.org/10.1016/j.cub.2013.01.051

Cognitive Neuroscience: TargetingNeuroplasticity with Neural Decodingand Biofeedback

New research combining neural decoding and biofeedback to targetneuroplasticity causally links early visual cortical plasticity with improvedperception. This is an exciting new approach to understanding brain function,one which may lead to new ways of treating neurological disorders by targetedintervention.

Aaron R. Seitz

A central goal of cognitiveneuroscience is to understand howbrains give rise to behavior. The holygrail of many fields of cognitiveneuroscience is to make causal linksbetween the processing within, or

between, various brain regions andpeople’s perceptions, decisions oractions. Establishing such causalitybetween brain and behavior isextremely difficult given that so manybrain regions are normally active duringtask performance, that correlationsbetween brain processing and

behavior can be spurious orepiphenomenal, and that thedirectionality of such correlations isalways ambiguous. Here we discusstwo new studies [1,2] that haveovercome these limitations by usinga novel approach combining neuraldecoding of functional magneticresonance imaging (fMRI) signals withbiofeedback to target neuroplasticitywithin specific brain regions.In the field of perceptual learning,

there has been a long and heateddebate regarding the role of early visualcortical plasticity in perceptual learning[3]. To date, the case for early visualcortex being important in behaviorallearning effects has been based uponcorrelational arguments, and whilethere are numerous demonstrations ofplasticity as early as primary visual

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Template defined

Decoded activity

A

B

Figure 1. Procedure for neuroplasticityexperiments based on neural decoding andbiofeedback.

(A) The first stage is to define template bydecoding stimulus inducted activity patternin the region of interest. (B) Participantsattempt to fill (blue disk) the entire circularregion (black circle) by inducing an activitypattern in the region of interest that matches(as determined by the decoder) the template.

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cortex (V1), the effects are typicallyinsufficient to explain the magnitude orpattern of behavioral results [4], andcomputational models show that mostbehavioral observations of perceptuallearning can be accounted for withoutrepresentational changes [5].

A fundamental difficulty inunderstanding the mechanisms ofperceptual learning is that manydifferent mechanisms can potentiallygive rise to the same behavioraloutcome. For example, in a typical taskof detecting a subtle orientation pattern(see pattern in Figure 1A), learningcould in principle be achieved by manypossible mechanisms; for example,reducing the system’s noise [6],increasing the gain of the signal [7],improving an internal template of thetarget [8], better attending the locationor features of the stimulus [9],improving decision rules regardingthe stimulus [10], and so on. Learningin a typical task includes contributionsfrommultiple factors, and each of thesemechanisms can involve plasticityin a variety of brain regions that areinvolved in accomplishing thatdetection task. This makes it verydifficult to understand the relationshipbetween the processes of an individualbrain area and the learning of a giventask.

But what if, instead of trainingparticipants to conduct a task, theyare trained to alter their brain activitythrough biofeedback? By targetingtraining to alter activity only in aspecific region of the brain, we canlearn about the function of that brainregion and its contribution to behavior.Shibata et al. [1] and Scharnowski et al.[2] recently employed this approachby training participants to alter theirbrain activity in early visual cortex,as assessed using fMRI decodingtechniques (Figure 1A), to matcha desired activity pattern. Shibata et al.[1] instructed participants to alter theirbrain activity to maximize the size ofa circle that was presented on screen(Figure 1B). Unbeknownst to theparticipants the size of the circle wasdetermined by the similarity of theparticipants’ brain activity in primaryand secondary visual cortex (V1/V2) tothat produced by viewing an orientedgrating pattern (see example inFigure 1A). Similarly, Scharnowski et al.[2] asked participants to alter their brainactivity to bring the level of a displayedthermometer to a high (up-regulatedstate) or low (down-regulated state)

target position. However, insteadof matching brain activity to astimulus-induced pattern, thethermometer height was determined bythe activity level of a targeted region ofprimary visual cortex (V1). Thus, in bothstudies, participants were requiredthrough trial and error to achievea mental state that was read-out usingfMRI decoding algorithms andcompared to a target-pattern(Figure 1B), determined by theexperimenter, and shown a feedbackstimulus (circle or thermometer) thatindicated their level of success atachieving the correct brain state.

Both studies show that trainingparticipants with biofeedback basedupon decoded neural signals can resultin perceptual learning. Shibata et al. [1]trained participants to repeatedlyactivate a particular activity patternin V1/V2, finding that this results inenhanced perceptual sensitivity to thestimulus matching the trained pattern.Similarly, Scharnowski et al. [2] trainedparticipants to up-regulate activityin a particular region of V1 andparticipants’ sensitivity improvedspecifically at the trained location, butonly when invoking the up-regulatedstate. Both studies report a number ofcontrol analyses which show thatdecoding signals from other brainregions could not account for theobserved behavioral learning effects.Thus, both studies demonstratea causal relationship between thealtered activity in early visual cortexand the observed behavioral changes.

Equally important is that differentmechanisms account for the observedlearning effects in the two studies.Shibata et al. [1] found that repeatedactivation of the target activity patternin V1/V2 resulted in improvedsensitivity, even without theparticipants activating this state duringthe post-training test, implicating localmechanisms of plasticity. Scharnowskiet al. [2] taught participants toup-regulate overall activity in theregion of interest and found thatthe improvement of sensitivity wasdependent upon participants being inthe up-regulated state. Furthermore,these authors used functionalconnectivity analysis to show that thisup-regulated state involved a networkbetween V1 and superior parietal lobe,a brain structure known to be involvedin the regulation of spatial attention.

Thus, while the two studies testedimproved discrimination of the same

type of stimuli (orientation patterns),the Shibata et al. [1] result is consistentwith a representation change in V1,whereas the Scharnowski et al. [2]result is consistent with improvedattentional focus to the trained regionof interest. These results suggest thatthese new imaging techniques can beused not only to target the role ofspecific brain regions in learning butalso to distinguish between differentmechanisms of plasticity involvingthese brain areas.Interestingly, in both studies [1,2],

unlike most studies of perceptuallearning, participants learned withoutviewing a specific stimulus duringtraining. Scharnowski et al. [2] informedparticipants of target location andinstructed them to engage in visualimagery at that location. Shibata et al.[1] provided no specific instructionsto their participants, though manyparticipants in that study also engagedin forms of mental imagery. Notably, inneither study did the participants’subjective report of their mental activitymatch up with the stimuli that theinvestigators used for testing. Still,using visual imagery to induceperceptual learning is an interestingapproach that has also shown success

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in other studies. For example,perceptual learning can be evokedthrough mental imagery of hyperacuitypatterns [11] or motion patterns [12]and results in similar training benefitsas those achieved through trainingon the same tasks with visuallypresented stimuli. Interestingly,training with imagined stimuli showeda similar degree of specificity to thecharacteristics of the imagined stimulias found through traditional trainingwith real stimuli. While it is unlikely thatthe task-related mental imageryresulted in the same type of focusedactivity pattern asmanipulated throughbiofeedback, it is likely that thereare some common mechanisms ofplasticity in these cases and suggestsan important role for mental imagery inperceptual learning.

Together, the two studies [1,2] showthat this new approach of usingdecoded neural signals as biofeedbackto induce targeted neural plasticity isa powerful way of identifying thefunction of individual brain regions aswell as neural networks involvingmultiple brain regions. Theseapproaches are particularly usefulin that they can support causalrelationships between brain activitypatterns and behavior. However,participants use unstructuredapproaches, such as mental imagery[11,12], to induce the target brainstates. This can give rise to significantindividual differences in outcomes [2],it is likely that there are changes in brainstate that are epiphenomenal to thosetargeted by the investigators, and thereare certainly differences in the learninginduced through biofeedbackcompared to that achieved throughtask performance. Thus, to gaina complete understanding of thehuman learning process biofeedbackwill need to be used in conjunction withstandard approaches.

These studies are not justscientifically interesting; they areexciting in their potential applications

to develop behavioral therapies forneurological disorders. Biofeedback[13] has had a long and mixed historyas a medical intervention, but hasalways held the promise that anindividual’s function can be improvedby learning to emulate the processesof a healthier counterpart. Newmethodologies using decoded neuralsignals as biofeedback to induce neuralplasticity [14] are advantageous in thatthey can be targeted to highly specificactivity patterns within and acrossbrain regions. Initial studies suggestpromise of these techniques in thetreatment of pain [15], emotionalregulation [16], social learning [17],tinnitus [18], and Parkinson disease[19]. While more research will berequired to determine the most optimaltraining conditions — for example, onlyhalf of Scharnowski et al’s. [2]participants learned the task — theappropriate target activity patternsto help individuals suffering fromdifferent conditions, and costs andaccessibility of the high-end fMRIfacilities used are currently prohibitiveto standard treatment, these studiesdemonstrate a very exciting future forfMRI-based biofeedback as targetedneuroplasticity-based therapy fortreating individuals with neurologicalconditions.

References1. Shibata, K., Watanabe, T., Sasaki, Y., and

Kawato, M. (2011). Perceptual learningincepted by decoded fMRI neurofeedbackwithout stimulus presentation. Science 334,1413–1415.

2. Scharnowski, F., Hutton, C., Josephs, O.,Weiskopf, N., and Rees, G. (2012). Improvingvisual perception through neurofeedback.J. Neurosci. 32, 17830–17841.

3. Seitz, A.R. (2011). Perceptual learning:stimulus-specific learning from low-level visualplasticity? Curr. Biol. 21, R814–R815.

4. Schoups, A., Vogels, R., Qian, N., and Orban, G.(2001). Practising orientation identificationimproves orientation coding in V1 neurons.Nature 412, 549–553.

5. Petrov, A.A., Dosher, B.A., and Lu, Z.L. (2005).The dynamics of perceptual learning: Anincremental reweighting model. Psycholog.Rev. 112, 715–743.

6. Dosher, B.A., and Lu, Z.L. (1998). Perceptuallearning reflects external noise filtering andinternal noise reduction through channel

reweighting. Proc. Natl. Acad. Sci. USA 95,13988–13993.

7. Gold, J., Bennett, P.J., and Sekuler, A.B. (1999).Signal but not noise changes with perceptuallearning. Nature 402, 176–178.

8. Li, R.W., Levi, D.M., and Klein, S.A. (2004).Perceptual learning improves efficiencyby re-tuning the decision ’template’ forposition discrimination. Nat. Neurosci. 7,178–183.

9. Franko, E., Seitz, A.R., and Vogels, R. (2010).Dissociable neural effects of long-termstimulus-reward pairing in macaque visualcortex. J. Cogn. Neurosci. 22, 1425–1439.

10. Yu, C., Zhang, J.Y., Zhang, G.L., Xiao, L.Q.,Klein, S.A., and Levi, D.M. (2010). Rule-basedlearning explains visual perceptual learning andits specificity and transfer. J. Neurosci. 30,12323–12328.

11. Tartaglia, E.M., Bamert, L., Mast, F.W., andHerzog, M.H. (2009). Human perceptuallearning by mental imagery. Curr. Biol. 19,2081–2085.

12. Tartaglia, E.M., Bamert, L., Herzog, M.H., andMast, F.W. (2012). Perceptual learning ofmotion discrimination by mental imagery.J. Vis. 12, 14.

13. Fetz, E.E., and Finocchio, D.V. (1971). Operantconditioning of specific patterns of neural andmuscular activity. Science 174, 431–435.

14. Weiskopf, N., Veit, R., Erb, M., Mathiak, K.,Grodd, W., Goebel, R., and Birbaumer, N.(2003). Physiological self-regulation of regionalbrain activity using real-time functionalmagnetic resonance imaging (fMRI):methodology and exemplary data. Neuroimage19, 577–586.

15. deCharms, R.C., Maeda, F., Glover, G.H.,Ludlow, D., Pauly, J.M., Soneji, D.,Gabrieli, J.D., and Mackey, S.C. (2005). Controlover brain activation and pain learned by usingreal-time functional MRI. Proc. Natl. Acad. Sci.USA 102, 18626–18631.

16. Johnston, S.J., Boehm, S.G., Healy, D.,Goebel, R., and Linden, D.E. (2010).Neurofeedback: A promising tool for theself-regulation of emotion networks.Neuroimage 49, 1066–1072.

17. Mathiak, K.A., Koush, Y., Dyck, M., Gaber, T.J.,Alawi, E., Zepf, F.D., Zvyagintsev, M., andMathiak, K. (2010). Social reinforcement canregulate localized brain activity. Eur. Arch.Psych. Clin. Neurosci. 260(Suppl 2 ),S132–S136.

18. Haller, S., Birbaumer, N., and Veit, R. (2010).Real-time fMRI feedback training may improvechronic tinnitus. Eur. Radiol. 20, 696–703.

19. Subramanian, L., Hindle, J.V., Johnston, S.,Roberts, M.V., Husain, M., Goebel, R., andLinden, D. (2011). Real-time functionalmagnetic resonance imaging neurofeedbackfor treatment of Parkinson’s disease.J. Neurosci. 31, 16309–16317.

Department of Psychology, University ofCalifornia, Riverside, 900 University Avenue,Riverside, CA 92521, USA.E-mail: aseitz@ucr.edu

http://dx.doi.org/10.1016/j.cub.2013.01.015