The Basal Ganglia and Adaptive Motor Control

Author(s): Ann M. Graybiel, Toshihiko Aosaki, Alice W. Flaherty, Minoru Kimura

Source: Science, New Series, Vol. 265, No. 5180 (Sep. 23, 1994), pp. 1826-1831
Published by: American Association for the Advancement of Science
Stable URL: http://www.jstor.org/stable/2884650 .
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 Single-unitstudiesof striatalneuronsare
The Basal Ganglia and Adaptive in accord with this general view, because
many of these neuronsexhibit highly con-
Motor Control text-dependentfiringpatterns(1 1, 16, 17).
They are active in relation to movements
triggeredby particularcues, includingmem-
Ann M. Graybiel,*ToshihikoAosaki, Alice W. Flaherty, ory-encodedcues as well as environmental
MinoruKimura ones. Most of the cells recorded in the
striatum are its projection neurons. It is
The basal ganglia are neural structures within the motor and cognitive control circuits in these projectionneurons,rather than the
the mammalian forebrain and are interconnected with the neocortex by multiple loops. rarerstriatalintemeurons,that degenerate
Dysfunction in these parallel loops caused by damage to the striatum results in major in Huntington'sdisease (18). By virtue of
defects in voluntary movement, exemplified in Parkinson's disease and Huntington's their differenttransmitterphenotypesand
disease. These parallel loops have a distributed modular architecture resembling local connectivity patterns, striatal projection
expert architectures of computational learning models. During sensorimotor learning, neurons may enhance or suppressmove-
such distributed networks may be coordinated by widely spaced striatal interneurons that ments throughbasalgangliapathwayswith
acquire response properties on the basis of experienced reward. inhibitoryand disinhibitory("release")ef-
fects on their thalamic and brainstemtar-
gets (9, 12, 19). Dysfunctionof these cir-
cuits is thus thought to produceeither hy-
During voluntary movement, large num- counterpartin coherent firing pattems re- pokinetic or hyperkineticbasalgangliadis-
bers of neurons in the forebrain and hind- latedto perceptualbinding.Relativelylittle orders(9, 12, 19).
brain become active. It is a major goal of informationis yet available about coordi- It has puzzledinvestigatorsfor yearsthat
research on the motor system to understand nated neuralfiring in motor circuits,how- there are millions of projectionneuronsin
the particular functions of individual corti- ever, and with the notable exception of the primatestriatum,but they projectto a
cal areas and subcortical sites in generating work on cerebellaroscillations (7), almost very much smaller set of neurons in the
volitional acts. Earlier views of cortical nothing is known about coherence in the basal ganglia output nuclei (20). Why
movement control emphasizing the primary subcorticalstructuresthat provideinforma- would striatalneuronshave such very spe-
motor cortex have now been augmented by tion to primaryand higher order motor cializedpropertiesif they simplyblendtheir
models that involve distributed coding corticalareas. outputsby convergingat the next step in
across multiple cortical areas, selective ac- A particularlyinterestingset of subcor- processing?Partof this puzzlewas resolved
tivation of cortical areas during the prepa- tical structuresare the basalganglia,which when it was discoveredthat there are mul-
ratory phases preceding movement, and dif- in the primatebrainforma massivecollec- tiple, parallel channels from the cortex
ferences in the degree of activation of cor- tion of neuronswith outputsmainlydirect- throughthe basal gangliaand back to the
tical areas before intemally guided and ed towardthe motorand prefrontalareasof cortex (8, 21). But this findingraisedother
stimulus-triggered movements (1). the frontal lobes, as well as towardsome questions:If informationis sent in parallel
Subcortical movement circuits, includ- brainstemmotor sites (8-11). Dysfunction throughthe basalganglia,whatdo the basal
ing the cerebellum and basal ganglia, also of the basal ganglia and the brain nuclei ganglia contributeto the processing?And
show large-scale changes in activation be- interconnectedwith them leads to distur- how are differentaspectsof the processing
fore and during motor activity (2). One of bancesof movementand cognition,includ- coordinated(the bindingproblem)?
the problems posed by such multilevel neu- ing disorderedtiming of movements (12, We focus here on two sets of findings
ral activity is the motor analog to the bind- 13). The anatomical circuit arrangement that suggestnovel approachesto these is-
ing problem in perception (3). How are within which the basal ganglia reside is sues. The first is evidence that the input-
brain circuits coordinated temporally and unique.Their largestinputstation,the stri- outputarchitectureof the sensorimotorstri-
spatially so as to produce coordinated motor atum, collects inputs from the entire neo- atum has a modular design that remaps
acts? cortex and sends processed information cortical inputs onto distributedlocal mod-
One interesting possibility suggested by throughother partsof the basal gangliato ules of striatalprojectionneurons.The sec-
recent work (4) is that synchronous or os- areasof frontal cortex that have been im- ond is evidence that the class of striatal
cillatory responses in motor cortical areas plicated in motor planningand execution. neuronsknown as tonicallyactive neurons
could underlie these functions in a way These striatalcircuitsare modulatedby the (TANs) may contributeto temporalbind-
analogous to that posited for synchronous dopamine-containing nigrostriatal tract, ing across such modularnetworksduring
firing and -40-Hz oscillations in the visual which degeneratesin Parkinson'sdisease. behavioral learning by undergoingdopa-
cortex and thalamus (5). Episodes of syn- The striatumalso receivesinputsfromtha- mine-sensitive changes in their response
chrony involving a broad range of frequen- lamic sites implicatedin rhythmicfiring in properties.
cies have also been observed (6), suggesting the forebrain(14) and from the amygdala,
that the distributed systems known by ana- which functions in reward leaming and Modular Remapping in the
tomical description might have a functional emotionalbehaviors,such as the expression Basal Ganglia
of fear (15).
A. M.GraybielandA.W.Flaherty areinthe Departmentof This arrangement,and the multiple in- An earlyhint that input-outputremapping
BrainandCognitiveSciences, MassachusettsInstitute
of
Technology,45 CarletonStreet, E25-618, Cambridge, temal loops of the basal have
ganglia, led to might occur in modules in the striatum
MA02139, USA.T.Aosakiis inthe Laboratory forNeural speculationthat the basal ganglia are not came from evidence that a dispersed set of
ControlResearchCenter,Institute simply related to motor execution per se.
Circuits,Bio-Mimetic neurochemically specialized patchy zones,
of Physicaland ChemicalResearch (RIKEN), 3-8-31
M.
Rokuban,Atsuta,Nagoya,Aichi456, Japan. Kimura Instead, they may in
participate motor plan- the striosomes, tend to collect inputs relat-
is at OsakaUniversity,
Facultyof Healthand SportSci- ning or predictivecontrol, motor sequenc- ed to the limbic system and to project to the
ences, Machikaneyama, Osaka560, Japan. ing, motor learning,and action repertoires dopamine-containing substantia nigra pars
*Towhomcorrespondenceshouldbe addressed. involvingmotivationaland cognitivedrive. compacta (9, 22). It is now clear, however,
1826 SCIENCE * VOL. 265 * 23 SEPTEMBER1994

that the entire striatumis modular.There
are input-outputmodulesin the largema-
trix compartment,and these "matrisomes"
receive sensorimotorand associativeinputs
andprojectto the outputnuclei of the basal
ganglia(23).
Studying the primate somatic sensory
and motor cortex, for example, we found
that the inputsderivedfromany smallcor-
tical site representinga particularbodypart
(say,the contralateralhand) forma distrib-
uted, partlyinterconnectedset of zones in
the striatum (24). Any given matrisome
receives overlappinginputs from the same
body-partrepresentationin differentsubar-
eas of the sensorimotorcortex, so that sev-
eral sorts of informationrelevant to that
body-partconverge.This suggeststhat the
cortical representationsof the body are
remappedin the striatumby being broken
up into local moduleswith convergentin-
puts (Fig. 1).
It is biologicallyexpensiveto set up such
patchy distributedsystems.This is not be-
cause they necessitateextra axonal length,
but because,in additionto implyinga gen-
eral topographyto organize the connec-
tions, they must also follow local con-
straintsthat breakthe rules of topography
|L F.'
3a 4 ning (30). In biological systems, we and
Fig. 1. Modularity of striatalinputsand outputs
documentedinan axontransportexperiment.(A)
An injectionof anterogradetracerwas made in a
smallsite in.the motorcortex(area4) representing
the foot (\). Inthe same hemisphere,a smallsite in
the pallidumwas injectedwith retrogradetracer
(7). Boththe labeledaxon projectionsfromcortex
to terminalsites inthe striatum(\) and the labeled
striatopallidal output cells (7) are organizedas
sets of patches in the putamen (B). The input
clusters and outputclusters overlapextensively
[cross-hatchingin(B)].Corticalrecordingsites (tri-
angles)andstimulation sites (circles)areshown in
the insetabove (A)(L,leg; F, foot;open symbols,
no response)for areas 3a and 4. ON, caudate
nucleus;P, putamen;GPi,internal segment of the
pallidum.
SCIENCE * VOL. 265
in orderto focusinputsinto specialmodules
(25). Why go to the expense?
One possible answer to this question
comes from experiments in which ana-
tomical tracerswere placed into monkey
brains to label simultaneouslysensorimo-
tor inputs to the striatum and striatal
outputs to the pallidum, a main output
structureof the basal ganglia. We found
that labeled input fiber clusterscan over-
lap clusters of labeled projection neurons
quite precisely(Fig. 1) (26-28). This sug-
gests a pattern of remappingin the basal
ganglia that involves divergencefrom the
cortex to the striatumfollowed by recon-
vergence from the striatum to the palli-
dum. In effect, the information is dis-
persed to distributedmodules in the stri-
atum,but it can be broughttogether again
at the next stage of processing (Fig. 2).
This divergence-reconvergence pat-
tern suggestsone way to have an overall
parallel processing scheme for cortico-
basal ganglia interactionsand at the same
time to maximize computational power
within channels. The estimated amount
of divergence and convergence is impres-
sive. The modules labeled from a roughly
1-mm-widesite in the sensorimotorcor-
tex stretch over as much as 7 mm of the
length and width of the putamen and fill
a volume three to five times the volume
of the cortical site from which they were
labeled. The striatalmoduleslabeled from
Neocortex
Striatum { ity in some neuropsychiatric disorders
DA
GP
I may be many sets of local expert modules,
SN
Fig. 2. Model of divergent-reconvergent process-
ing in basal ganglia pathways. Experimental evi-
dence favors the divergence of cortical inputs to
modules in the striatum. Any given module can
receive somatotopically matched inputs, symbol-
ized by F (foot), from differentSI areas (areas 3a,
3b, and 1) and from the motor cortex (area 4). This
divergence can be followed by reconvergence
onto sets of basal ganglia output cells in the palli-
dum (GP). Inputs from the midbrain substantia
nigra(SN) using the neurotransmitter
dopamine
(DA)modulatethis processing,as do local inter-
neurons(smalldots).
* 23 SEPTEMBER1994
ARTICLES
a given small site in the pallidum have
about the same dimensions (26-28).
Such dispersion is great enough so that
the individual modules in any one input-
output set could have different nearest
neighbor relations. This design thus fa-
vors local spatiotemporalcoherencewithin
individualinput-outputmodulesas well as
diversity across them, which could allow
plasticityand variabilityin striatalprocess-
ing. Individualmodulesmight also be sub-
ject to differentpatternsof within-module
convergence(forexample,differentdegrees
of submodalityconvergence)andbe subject
to different sorts of local processing(for
example,reflectingdifferentneurochemical
environments).This wouldfurtherincrease
the possibilityof dynamicprocessingin ap-
parentlyparallelchannels.
There is a provocative similarity be-
tween this biological architectureand the
network architectureproposed by Jacobs
and colleagues for a supervised learning
system (29). The input-output modules
resemblethe "local experts"of their mod-
el, which are subsets of elements that
perform distinct subtasks of a training
routine and which therefore split up the
computational problem. The outputs of
these local experts can be independently
adjusted and gated and then summed at
an output stage. This architectureshould
have advantagesfor dealing with the de-
grees-of-freedomproblem in motor plan-
others find input and output modules
throughout the striatum, not just in the
sensorimotorstriatum (23). For example,
in the head of the caudatenucleus, which
has been implicated in higher order cog-
nitive functions and has abnormalactiv-
(31 ), this local clusteringphenomenon is
very pronounced,and the limbic system-
related striosomalmodules are most con-
spicuouslyrepresentedthere. Thus, there
with some, probablyincluding striosomes,
serving nonsensorimotor functions, and
there may be different sorts of nearest
neighbor relations among the modules as
well. These input-output modules in the
striatum may be one alternative to the
multilayerprocessing typical of the neo-
cortex (32).
These computational considerations
suggestthat local processingorganizedwith
respectto matrisomaland striosomalmod-
ules may be a key featureof input-output
remappingin the striatum.Buthow can the
activity in differentconstellationsof mod-
ules be coordinated?Studyingthe physio-
logicalchangesthat occurin a particularset
of striatal neurons during behavior learning
in the monkey, we found evidence for one
potential solution to this problem.
1827
 Tonically Active Neurons and
Striatal Neuroplasticity
The TANs of the striatum, thought to be
intemeurons (17, 33), are rare striatal neu-
rons that fire "spontaneously" at low (2 to
10 Hz) frequency. Unlike many projection
neurons, the TANs do not fire in relation
to overt movement. By recording their fir-
ing patterns during the course of classical
conditioning, we found that these cells un-
dergo changes in responsiveness during the
conditioning (34).
In tasks in which conditioning stimuli
(clicks or lights) were pairedwith rewardpre-
sentations (fruit juice), the monkeys leamed
to respond behaviorally (by licking) to re-
ward-associatedconditioning stimuli. During
acquisition of conditioning, the TANs devel-
oped a pause in their tonic firing, often
flanked by brief excitatory phases, which
came shortly after the click or light (Fig. 3).
The number of responding TANs increased over, the TAN responseoffsets were tem-
from about 15% before conditioning to over
50 to 70% after conditioning.
The increase in the population response
represents a gradual recruitment of respon-
sive TANs during the course of behavioral
conditioning and a lengthening of their
responses (35). These responses clearly were
related to conditioned stimuli predictive of
reward, because they disappeared when the
animals underwent extinction training, dur-
ing which the stimuli were presented with-
out reward. The TANs did not respond to
the rewards alone, however, nor in relation.
to the licks made to acquire the reward.
As an estimate of the temporal precision
of the TAN responses after learning, we
calculated coefficients of variation (CVs)
for the pause responses of individual TANs
and compared these to the CVs for the base
line interspike intervals of the TANs (35).
Fig. 3. Emergence of Striatum(TANs)
population responses of
TANs in the striatum dur-
ing a classical condition- Before
ing task in which the _
conditioning
monkey learns to associ-
ate the presentation of a
click with a juice reward
that the animal can ob-
tamnby licking. (Left) 118dyI
Population histograms Yo
of TANs before, during,
and after behavioral
learning. The neurons
show an initialactivation,
then a reduction in firing, 9 to 21 days ,
and then a rebound exci-
tation. (Right) The corre-
sponding acquisitionof
the conditional behavior-
al response (licking).As the monkey learns the conditioned response, the TANs acquire a response to the
conditioning stimulus. The numbers in parentheses indicate the number of neurons sampled. EMG,
electromyogram.
1828
This analysis demonstratedthat a highly rochemicallydetected within the matrix,
significant coordinationof TAN activity TANs could be found by them as well.
occurs after learning. The onsets of the These resultssuggestthat the distributionof
pausesthat developedshowedconsiderable the TANs, althoughverybroad,is not ran-
temporalalignment,and the offsetsof the dom and may be related to the modular
pauses(and onsets of reboundexcitations) organizationof the striatum(Fig. 5). Ap-
were also closely correlatedin time (36). proximatelyhalf the TANs identified in
One speculationsuggestedby these findings acute recordingexperimentsin the squirrel
is that the pausein TAN firingthat devel- monkey striatum lay at striosome-matrix
ops afterlearningmay representa resetting borders.These TANs could link limbic in-
of the spikedischargeimposedby a suppres- formationwith informationof other types
sion of the TANs followedby a time-locked (for example,that derivedfrom frontalas-
resumptionof their activity (a "latch-on") sociation cortex) in a coordinated,distrib-
afterthe inhibition (35). uted way (35, 37).
The fact that TANs distributedover
Modules, TANs and the broadregions of the striatumcome to re-
Binding Problem spondin a temporallycoordinatedwayafter
behavioralconditioningsuggeststhat these
A remarkablefeatureof the change in neu- striatalneuronscouldfacilitatecoordinated
ralfiringof TANs accompanyinglearningis changes in the activity of other striatal
that it occurredin TANs very widely dis- neurons,includingthe projectionneurons,
persedthroughthe striatum(Fig.4). More- during learning. Even modules stretching
acrossmillimetersof striatumand forming
porallycoordinatedindependentof wheth- partsof different"parallel"circuitscouldbe
er they lay in striatal districts receiving affected.In the striatum,then, the binding
inputs predominantlyfrom the sensorimo- problemimposedby the modularorganiza-
tor cortex (much of the putamen) or in tion of the striatum,by its divergentinput
regions with inputs predominantlyfrom architecture,and by the presenceof parallel
prefrontal and other association cortex basalgangliachannelsrunningthroughthe
(much of the caudatenucleus). striatumcould be solved by having distrib-
This broaddistributionand temporalco- uted sets of neurons(almostcertainlyinter-
ordinationof the TAN responsesuggested neurons) that coordinatethe modules,in-
that TANs mighthave a specialfunctionin puts, and loop activities.
coordinatingthe distributedmodularcir- This proposalsuggestsa novel solutionfor
cuitryof cortico-basalgangliachannels.To part of the bindingproblemin the sensori-
test this idea, we explicitly mapped the motorsystem.Ratherthanhavingall systems
locations of TANs with respect to the synchronouswith each other, the coordina-
chemically defined striosomes,which we tion is a contingentcoordination,built up
could detect with immunohistochemical throughleaming and implemented,in the
stains (35). There was a pronouncedten- caseof the striatum,bydistributedsetsof local
dency for TANs to lie at striosome-matrix neuronssensitiveto motivation-related sig-
borders.Moreover,in some of the rare in- nals.SimultaneousmultipleTAN recordings
stances in which boundariescould be neu- will be necessaryto judgehow synchronous
the TAN responsesare.However,ourresults
alreadysuggestthat their effects could be
EMG(licking) withinthe summationtimesof theirpotential
Spikes/s targetneurons(38, 39) and that the pause
(83) 15 - _- overlapscouldbe sufficientlyalignedto create
a time window in which TAN activity is
coherentlydiminished(40).
L -
Spikes/s Binding, Reward, and
(69) 15 Striatal Dopamine
| The rewardassociation of the TAN re-
0 sponse acquiredthroughconditioningsug-
gested a furtherexperimentbased on evi-
pikes/s dence obtainedby Schultz and co-workers
(4 1
(41). These investigators have shown that
_____________
the dopamine-containing neurons of the
substantia nigra, which project to the stri-
-_A
1s atum, fire in response to primary rewards
Click Click and, after conditioning, to reward-related
stimuli. To determine whether these do-
pamine-containing fibers influence TAN
neuroplasticity, we destroyed these fibers
SCIENCE * VOL. 265 * 23 SEPTEMBER1994
 'ER ARTICLES

unilaterallyby local infusionof the neuro- ly nearlysilent neuronswill occur (44). pauseplus a reboundin TAN firing could
toxin 1-methyl-4-phenyl-1,2,3,6-tetrahydro- Interestingly,muscariniccholinergicre- serve as a temporallycoordinatedsignal to
pyridine(MPTP) into the striataof mon- ceptor agoniststend to stabilizethe up or reset the activity states of projectionneu-
keysthat had learnedthe conditioningtask. down states of projectionneuronsby mod- ronsoverwidespreadregionsof the striatum
When the dopamine-containing fiberswere ulationof A-currents(45). If the TANs are (35). Over time, throughthe gradualacqui-
destroyedin one hemisphere,the monkeys cholinergic intemeurons, a coordinated sition of time-lockedconditionedresponses
could still perform (albeit clumsily) the
lickingtask,which requiredmuscleactivity
on both sides.However,mostTANs on the Spikes/s Spikes/s
-30 30
side of the infusion lost their pause re-
sponse, even though their tonic activity 0~ ~~~~~~~~~3
seemed normal.The TANs in the control ILLE -1&,,
i ~-5 w E15
hemisphere,by contrast, continued to re-
spond. These experimentsstronglysuggest
that the expressionof the acquiredresponses
of the TANs requirestonic dopaminergic
input.Moreover,systemicinjectionsof apo-
morphinecould reinstatethe responseslost -'CN/
on the side of the infusion,which suggests
that the dopaminesignalneededforexpres- Spikes/s A15 Spikes/s
sion of the responsemay be spatiotempo- -30 ,< 'A 730
rallypermissive(42).
w&1t5 "'A17 wh/A5
Striatal Activity and 0 .
Sensorimotor Learning
The experimentsdescribedabove suggest
that duringconditioning,striatalTANs de-
velop a responsethat is spatiallydistributed, /<H \S~~~~~
temporallycoordinated,predictive of re- - /> g 9 ~~~~~P
Ah21
ward,and dependenton dopamine.What
Spikes/s \> Spikes/s
could such a neuralsignal accomplish?An r30 * 30
impedimentto answeringthis question is
that the cellularphenotypeof the TANs is Li 491 11L
-~15 j| | 4 f i 15
not known. However, their electrophysi-
ologicalpropertiespoint to their being stri-
atal intemeurons, and in particulartheir
broadaction potentials,prolongedafter-hy-
perpolarizations, and tonic firingcloselyre- 1 ms
semble propertiesof cholinergic interneu-
Fig. 4. Similarityof pause responses acquired by TANs in widely spaced regions of the striatumas a result
rons and do not resemblethose of projec-
of conditioning with clicks and light-emittingdiode (LED)lights as conditioned stimuli.The responses of
tion neurons or noncholinergic interneu- six representative TANs recorded at particularsites (indicated by dots or squares) are shown in individual
rons, as identifiedin studiesin the rat (38, raster plots and spike histograms. Despite their widespread distribution,all of the cells show a pause
43). Our finding that TANs are differen- response after the presentation of one or both of the stimuli used as conditioning stimuli (0, cell that
tially distributedat striosomalbordersand responded to both; V, responsive cell that was tested only with a click).
arestronglyrepresentedin the matrixis also
compatiblewith the view that TANs could
be cholinergicinterneurons(35). Fig. 5. Preferential distribution of
In sharpcontrastto the TANs, striatal TANs in the matrixand at the edges
of striosomes. Shown are strio-
projection neurons are peculiar in being somes (irregularshaded forms) in
almost completelysilent in the absenceof nine serial sections from a squirrel
movement or equivalent activation. But monkey striatum, reconstructed in
once they are broughtto firing threshold, three dimensions and plotted to-
they exhibit burstsof firing (38, 39). They gether with the sites of TANs (red
tend to be in "up"or "down"states and to dots) marked in acute recording ex-
flip between them. It is likely that the periments in this monkey. A dispro-
burstlike projection neuron firing, rather portionate number of TAN sites lie
than the smallmodulationsof TAN firing, at striosome-matrix borders; others
lie in the matrixand may be at ma-
contributesthe immediatetransferof neural trisome-matrisome borders.
informationto striataloutputtargetsin the
pallidum and substantianigra. However,
the TANs could have a considerableinflu-
ence on the subthresholdpotentialsof pro-
jection neurons, potentials that are of great
importance in determining whether and
when the burstlike activity of these normal-

SCIENCE * VOL. 265 * 23 SEPTEMBER1994 1829

duringrepeatedexposureto particularbe-
havioral contexts, TANs could come to
influencethe probabilityof the firingof sets
of surrounding neuronswhen these neurons
contemporaneouslyreceive inputs related
to the stimulus-responsecontext. The
short-termmodifiabilityintroducedby the
latch-on function could thus have long-
term effects.
The scheme of striatalprocessingthat
we proposehas elements of both unsuper-
vised (Hebbian) and supervisedlearning
models (46). Within local striatalmodules,
the degreeof temporalcoherenceof inputs
to the projectionneuronscould determine
input-output functions with Hebbian
mechanismsacting in adjustmentsof syn-
aptic strengths(47). In addition,however,
the learningwouldbe supervised:The mod-
ifiabilityof any given moduleat any partic-
ular time point would be influenced by
distributedinterneuronsactive in a condi-
tional spatiotemporalgatingof the activity
in the distributedmodules.
The response of the TANs to condi-
tioned stimuli fits well with the idea that
the striatumis involved in predictivecon-
trol:The cells modulatetheirspike activity
in relationto stimulithat are predictiveof
reward.Their change in responsivenessis
also compatiblewith the idea that the stri-
atum is involved in some aspectsof senso-
rimotor learning (48), because their re-
sponsesundergochangeswith conditioning
as the monkeylearnsthe behavioralsenso-
rimotortask.Our evidence that TAN plas-
ticity is modulatedby dopamineis in turn
compatiblewith a "teaching"role for re-
ward-relatednigrostriataldopaminergicin-
put (49), and it mayhelp in understanding
the remarkablesuccess of dopamine re-
placement therapies in facilitating the
movementsof patientswith Parkinson'sdis-
ease (50). More generally,it is of interest
that numerouspharmacologictherapiesfor
basal ganglia disorderstarget cholinergic
and dopaminergicsystems (51). Both sys-
tems have also been implicatedin striatal
synaptic plasticity in studies of long-term
depressionandlong-termpotentiation(52).
The predictionfrom our analysiswould be
that not only difficultiesin motorlearning
or predictivecontrol,as in sequentialmove-
ment planning,but also difficultiesin tim-
ing complex movements and even cogni-
tive and psychomotorbehaviorscould re-
sult fromreducedtemporalcoordinationof
activity in the modulardistributedcircuits
discussedhere.
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 RESEARCH ARTICLE

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53. Supported by Javits Award, NIH grants NS25529
and NEI 02866, the Human FrontierScience Pro-
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M. Johnson, who produced the image in Fig. 5.

wavelengthsnear 226 nm. The newly de-

RESEARCHARTICLE veloped techniqueof photofragmentimag-
ing has been used to measurethe velocity
distributionof the O(3P) product;conser-
The "Ozone Deficit" Problem: vation of energy and momentumprovide
the internalenergyof the 02 sibling frag-
02(X, v 26) + O(3i) from ment. In addition, laser-inducedfluores-
cence (LIF)on the Schumann-Runge bands
226-nm Ozone Photodissociation has been performedto determinethe distri-
bution of 02 (X3V-, v) populationin the
vibrationallevels between v = 19 and v =
R. L. Miller,A. G. Suits, P. L. Houston, R. Toumi,*J. A. Mack, 26. The experimentstaken together indi-
A. M. Wodtke cate that the vibrationaldistributionof the
02(X3Eg-, v) produced at this dissociation
Highly vibrationally excited O2(X3yg, V 2 26) has been observed from the photodis- wavelengthis markedlybimodal,with one
sociation of ozone (03), and the quantum yield for this reaction has been determined for peak near v = 14 and anotherat v = 27.
excitation at 226 nanometers. This observation may help to address the "ozone deficit" The chemistry of 03 has come under
problem, or why the previously predicted stratospheric 03 concentration is less than that increasingscrutinylargelybecauseof con-
observed. Recent kinetic studies have suggested that 02(X 3>g-, v ? 26) can react rapidly cern about stratospheric03 loss due to
with 02 to form 03 + 0 and have led to speculation that, if produced in the photodis- human activity. Production of strato-
sociation of 03, this species might be involved in resolving the discrepancy. The sequence spheric 03 is believed to be due solely to
03+ hv > 02(X3Eg-, v 2 26) + 0; 02(X3 g-, v 2 26) + 02 -> 03+ 0 (where hv is a reaction 1:
photon) would be an autocatalytic mechanism for production of odd oxygen. A two-
02+hv -> 20 (1)
dimensional atmospheric model has been used to evaluate the importance of this new
mechanism. The new mechanism can completely account for the tropical 03 deficit at an (whereh is Planck'sconstant),which then
altitude of 43 kilometers, but it does not completely account for the deficit at higher rapidlygenerates03 in excess 02 through
altitudes. The mechanism also provides for isotopic fractionation and may contribute to three-bodyrecombination:0 + 02 + M --
an explanation for the anomalously high concentration of heavy 03 in the stratosphere. 03 + M (M = 2 or N2). Decomposition of
03 is due to two photochemicalpathways:
03+hv >0(1D) + 02(a1lAg) (2)
Attempts to predict the stratospheric03 + 0, this sequenceof reactionsmight pro- >0(3P) + 02(X3E9;) (3)
concentration date historically to Chap- vide a meansfor formationof stratospheric
man'spioneeringworkin 1930 (1). Despite 03 (3-5). The workdescribedhere demon- as well as to three catalyticprocessescom-
years of effort, there is still a significant stratesthat highly vibrationallyexcited 02 monly referredto as the HOx, NOx, and
discrepancy between the predicted and is indeedformedin the photodissociationof ClOxcycles (7). Notwithstandingthe large
measured03 concentration in the upper 03. The quantumyield of this reactionhas number of previous attempts (8-23),
stratosphere(2). It has recently been pro- been determinedso that the importanceof models of stratosphericchemistry under-
posed that if the 02 producedin 03 pho- the mechanismproposedin (3-5) can be estimate the concentration of 03 when
tolysiswere sufficientlyvibrationallyexcit- evaluated.Calculationsshow that the in- compared to observations at altitudes
ed to reactwith ground-state02 to form03 clusionof highlyvibrationallyexcited?2 in between 35 and 80 km (2, 24, 25). This
atmosphericmodels may help resolve the discrepancy is particularly puzzling be-
R. L. Miller,A. G. Suits, and P. L. Houston are with the long-standing03 deficit problem.In addi- cause 03 is in photochemical steady-state
Department of Chemistry, Cornell University,Ithaca, NY,
USA 14853-1301. R. Toumi is with the Centre for Atmo- tion, the new dissociationmechanismin- during daylight hours at these altitudes
spheric Science, Department of Chemistry, Lensfield volving vibrationallyexcited ?2 may also and its abundanceis controlled by such a
Road, Cambridge CB2 1EW, United Kingdom. J. A. be involved in resolvingthe long-standing small number of well-studied chemical
Mack and A. M. Wodtke are with the Department of
Chemistry, University of California,Santa Barbara, CA, mysteryof why heavy isotopes of 03 are and photochemical reactions.
USA 931 06. more abundantin the stratosphere(6). There have been at least two notable
*Present address: Department of Physics, ImperialCol- Two new experimentswereperformedto attempts to explain the so-called "ozone
lege, London SW7 2BZ, United Kingdom. explore the photodissociation of 03 at deficit"problem,each hypothesizinga sec-
SCIENCE * VOL. 265 * 23 SEPTEMBER1994 1831