ing 10 mM bic was placed within the forelimb area,
0.5 to 2.0 mm lateral to the stimulating electrode ata depth of 1.8 mm (layer V). In some experiments a
glass multibarrelled micropipette was used for the
separate application of bic, ACh, or glutamate. The
bic was ejected continuously (50 to 150 nA) at thisforelimb site for 7 to 80 min, while movements and
EMG evoked by stimulating at the vib test site wererecorded at 5- to 15-min intervals.
10. In 12 of the 15 rats, multiple bic applications were
made. Second and third applications were made only
after the shift was no longer observed. Each application produced the same reorganization.
11. A. Iriki et al., Science 245, 1385 (1989).
12. We applied 0.3 FM (-)[3H]bicuculline methyl
chloride through our usual glass pipettes with +5
nA for 2 hours.
13. Sections of unfixed tissue were exposed to autoradiographic film and then developed. Radioactive

labeling was measured by a computer-based densitometer. The decrease in labeling density from thecenter of the application site fit a Gaussian distribution reaching two standard deviations below thepeak value 600 gm from the ejection center.
14. Threshold SEM for vibrissa movement were 28.1
2.6 LA, pi = 43, before and 33.3 2.2 ipA, n =65 (not significant, P > 0.05, t test), after bic±±±

application.

15. Acetylcholine chloride (0.5 M) was applied withcurrents of 50 to 150 nA and sodium glutamate (0.5M) was applied with 25 to 150 nA.
16. R. Metherate, N. Tremblay, R. W. Dykes, J. Neurophysiol. 59, 1231 (1988).
17. K. Krnjevic and J. W. Phillis, J. Physiol. (London)
166, 296 (1963).
18. J. P. Donoghue and K. L. Carroll, Brain Res. 408,
367 (1987).
19. The marked increase in discharge rate of layer V

DI Dopamine Receptors in Prefrontal Cortex:
Involvement in Working Memory
TOSHIYUKI SAWAGUCHI AND PATRICIA S. GOLDMAN-RAKIC
The prefrontal cortex is involved in the cognitive process of working memory. Local
injections of SCH23390 and SCH39166, selective antagonists of the Dl dopamine
receptor, into the prefrontal cortex of rhesus monkeys induced errors and increased
latency in performance on an oculomotor task that required memory-guided saccades.
The deficit was dose-dependent and sensitive to the duration ofthe delay period. These
Dl antagonists had no effect on performance in a control task requiring visually guided
saccades, indicating that sensory and motor functions were unaltered. Thus, Dl
dopamine receptors play a selective role in the mnemonic, predictive functions of the
primate prefrontal cortex.
IN NONHUMAN PRIMATES, THE PRE-

frontal cortex (PFC), in particular its
dorsolateral region, is critical for thecognitive process of working memory (1).
Several lines of research suggest that dopamine (DA) may influence this process. The
concentration of DA in the PFC is among
the highest in all cortical areas in monkeys(2), and both DA-containing fibers and DA
receptors are prominent in the primate PFC(3, 4). Local depletion of DA in the PFC ofmonkeys induces impairment in tasks that
require delayed response (5), and neuronal
activity related to delayed response performance is augmented by iontophoreticallyapplied DA (6). These findings suggest that
DA receptors may be involved in the mnemonic processes of the PFC.
There are two types of DA receptors in
the central nervous system, Dl and D2
receptors (7); the PFC of primates, inclu 1ing humans, contains a high level of D.
receptors (4, 8, 9) and a relatively low or
negligible level of D2 receptors (4, 9, 10).
These findings imply that the Dl receptors
are likely to be involved in the mnemonic
process mediated by the PFC, but direct
Section of Neurobiology, Yale University School of
Medicine, New Haven, CT 06510.
22 FEBRUARY 1991

evidence is lacking. This hypothesis can now
be directly tested by the use of potent Dland(11)
antagonists, SCH23390
SCH39166 (12), in combination with sensitive behavioral paradigms for assessing
working memory.
We used an oculomotor delayed-response(ODR) task in which animals were trained
to fixate a central spot on a cathode-ray tube
while a visual cue was presented briefly in
one of several (6 to 22) locations in thevisual field. The cue then disappeared, andafter a 1.5- to 6-s delay the animal wasneurons during ACh or glutamate application is themeasure of a general increase in excitability de-scribed here.
20. N. D. Akhtar and P. N. Land, Neurosci. Abstr. 13,
77 (1987); S. H. Hendry and E. G. Jones, Nature
320, 750 (1986); E. Welker, E. Soriano, H. van derLoos, Exp. Brain Res. 74, 441 (1989).
21. M. McCarren and B. E. Algerj. Neurophysiol. 53,
557 (1985).
22. A. Stelzer, N. T. Slater, G. T. Bruggencate, Nature
326, 698 (1987).
23. H. Wigstrom and B. Gustafsson, Acta Physiol.
Scand. 125, 159 (1985).
24. Y. Chagnac-Amitai and B. W. Connors, J. Neurophysiol. 61, 747 (1989).
25. This work was supported by March of Dimes grant
1-1169 and NIH grants NS22517 and NS25074.
30 July 1990; accepted 28 November 1990

required to make a memory-guided saccade
to where the target had been presented
seconds before. Therefore, to achieve criterion performance on the ODR task theanimal had to remember visuospatial data inorder to make the correct response at theend of the delay. To distinguish a deficit inmnemonic function from deficits in eye
movements or sensory perception, we used acontrol procedure in which the target remained on during the delay period and thesubject made a sensory-guided saccade to
the target. Neuronal activity in the dorsolateral PFC of monkeys is involved in the
ODR task (13), and lesions of the dorsolateral PFC induce deficits in the memoryguided saccades required by the task (14).
However, to examine the role of neurotransmitters or receptors on specified cortical
functions, a method of targeting specificbrain regions was required. Therefore, we
combined the ODR paradigm with the intracerebral injection of SCH23390 and
SCH39166 and now report that the activation of Dl receptors plays a critical role inthe mnemonic process mediated by the primate PFC.
Three rhesus monkeys (T, J, and N) weretrained in the ODR and control tasks (15).
Fig. 1. Injection sites of SCH23390 and
SCH39166 in two of the monkeys illustrated ona lateral view of the left PFC. The sites werereconstructed in reference to cortical sulci. Dataon injection sites in one monkey, N, that has not
yet been killed are not included. However, theeffective sites in this monkey are distributed in thesame region on the basis of the position of thecylinder and the coordinates of the micromanipulator used for injections; 0, effective sites of
SCH23390 on ODR performance; ], effective
sites of SCH39166 on ODR performance;
ineffective sites with either drug. The number ofthe injection site in Fig. 1 corresponds to theinjection site shown in Table 1. PS, principal
sulcus; AS, arcuate sulcus. Injections were placed
2 to 4 mm deep to the dural surface; no sites werelocated within the banks of the principal sulcus.
U,

REPORTS947

Fig.2.TheeffectoftheDl

A
ODR

ODR/-

1

Post

Pre

antagonist SCH23390 on
the oculomotor delayed-response (ODR) and control(CON) tasks. SCH23390(50 jg) was injected into

the left PFC (site 1 in Table0a total of six locations that

300

-20

1). The cue was presented atwere separated by 450 or 900
in direction, and their eccen-

0

20

40

60

80

E

CON

tricity was 200. (A) Superimposition of two-dimen--h

a

. 10

N

fi1

B
a
20
15.O +

y

250

250

@

...200sional trajectories of thesaccade to each target in the
ODR and CON tasks. Pre,10deg 0 150-20 0 20 40 60 80
before injection; Post, 10 toTime after injection (min)20 min after injection. Afterthe injection, the variability
and discrepancy between target and memory-guided saccades made to it increased for a specific target
located at the lower right (dashed trajectories). (B) Time course of changes in the accuracy (top) andthe onset latency (bottom) of the saccade for the ODR task and CON tasks. The data are for trials at
the location indicated by the arrow (inset). Mean ± SEM; n = 4 to 7 trials per time point.

Table 1. Onset latency of the response for each injection site that was associated with a deficit on
the ODR task after injection of SCH23390 or SCH39166. The data given for each injection are forthe target affected most strongly and for the postdrug block or blocks for which the score wassignificantly different from the predrug score. Data for 5- to 6-s delays are shown. Scores before andafter injection were compared by analysis of variance, and multiple comparisons were made with theNewman-Keuls procedure (17). The number of trials is shown in parentheses. Injections labeled a,b, c, and d were placed with the same coordinates as those used for injections 4, 10, 11, and 16,
respectively. *, P < 0.05; **, P < 0.01.
Injection
site(Fig. 1)

Onset latency (ms) (mean + SD)

Dose
1g

(kg)

Predrug

Postdrug

SCH23390

Monkey T
1
2
3
3
3
4
5
6
7
8
9
9
9
10
11

50
30
60
30

15
30
20
10
30
10
60
30
15
80
30
15

Monkey J
12
12
13
14

Monkey T
18a
19

20b
21c
Monkey N
22d
23
23
24
948

269.9 + 47.4**(11)282.0 ± 48.1**(12)256.2 ± 21.2**(10)240.6 13.7**(11)224.6 11.8**(9)262.2 ± 24.7**(5)248.9 15.7**(15)234.4 10.0**(10)242.4 ± 12.9**(14)235.9 ± 23.2*(8)259.4+ 18.3**(8)240.4 19.3**(10)230.9 28.0*(8)260.7 25.0**(17)249.0 ± 25.2**(7)227.5 ± 20.0**(13)

SM)
°

0

400

DOE~~~~

.00
A

z 300
at

p1

0

A

200
o

lo10'

5

10

15

20

25

Amplitude (deg)

60
30
30
30

209.7 17.7(11)206.6 19.8(7)195.0 ± 8.5(7)194.1 ± 22.8(10)302.0 52.5**(13)257.2 37.0**(10)244.5 ± 31.6**(10)258.3 ± 19.5**(11)

30
30
30

238.6 ± 10.6(12)239.4 ± 24.4(12)228.0 ± 10.8(9)SCH39166

292.7 ± 32.2**(15)313.6 ± 36.8**(15)249.5 ± 24.2**(12)

5
5
5
1

199.1 ± 8.2(14)207.8 ± 17.6(10)199.7 ± 10.3(10)205.2 ± 13.4(10)221.3 ± 8.0**(9)272.0 ± 43.0**(10)227.0 ± 10.7**(11)

10
10
5
5

231.8 ± 10.3(14)233.7 ± 23.3(9)247.3 ± 13.7(14)243.0 ± 7.2(8)277.7 ± 19.7**(10)304.5 ± 37.5**(10)274.0 + 28.9**(12)280.6 ± 17.2**(11)Monkey N
15
16
17

195.9 ± 11.4(8)197.6 ± 28.2(10)208.8 ± 15.0(10)208.5 ± 10.6(8)203.5 ±4.8(8)180.8 ± 8.0(4)202.6 16.2(14)212.4 14.1(10)198.4 ± 14.1(9)211.6 ± 21.8(10)198.6 19.2(11)193.8 ± 11.6(10)206.1 + 7.9(9)203.6 ± 15.6(10)196.3 ± 15.2(7)202.2 ± 16.9(10)While the monkey performed these tasks, 3
gI of SCH23390, SCH23388, ketanserin,
or SCH39166 was injected locally into thedorsolateral PFC with a 10-[uL Hamilton
syringe (16). The injection of SCH23390(10 to 80 pug) induced reversible deficits in
ODR performance in all three monkeys at a
total of 17 sites in the principal sulcal regionof the dorsolateral PFC (Table 1 and Fig. 1)(17). The impairment was quantified as anincrease in error, measured by the discrepancy of the position of the to-be-remembered target and the saccade performed by
the monkey at the end of each trial (Fig. 2)
and by an increase in latency to respond(18). The trajectories of the saccades wereabnormal (Fig. 2A), although their velocity
did not change (Fig. 3). These deficits usually occurred within 10 min after the injection (in most cases, within 1 to 3 min after
the injection), reached a peak at 20 to 40
min, and recovered at 60 to 90 min after the
injection (Fig. 2B). The change in performance was restricted to a few specific target
locations, which varied with the injection
site and were usually contralateral to it. By
contrast to the performance of the ODRtask, we observed no significant changes in
the performance of the control task after the
injection of SCH23390 during the same
experimental session in which performanceon the ODR task was impaired (Fig. 2). The
accuracy and onset latency of sensory-guid-

231.0 ± 18.6**(11)Fig. 3. Relations between amplitude and velocityof the memory-guided saccades in the ODR task
before and after injection of SCH23390.
SCH23390 (30 jig) was injected into the left
PFC while the monkey performed the ODR task;
discrepancy and onset latency of memory-guided
saccades to a target location were significantly
increased after the injection (site 13 in Table 1).
The cue was presented at a total of 22 locations
that were separated by 450 or 900 in radial direction, with eccentricities of 7, 130, and 200. The
velocity was plotted as a function of the amplitudeof the saccade for each trial. The data are for trials
at the three locations with the same direction
indicated by closed squares (inset). The memoryguided saccades in this direction were those moststrongly affected by the injection; 0, before injection; A, 10 to 40 min after injection. The relation
between amplitude and velocity was similar before and after the SCH23390 injection.
SCIENCE, VOL. 251

ed saccades in the control task were the same
before and after the injection for all target
locations. Furthermore, the deficit in the
ODR task induced by SCH23390 was sensitive to the duration of the delay period,and longer delays were associated with larger errors (Fig. 4A). Moreover, the degree ofthe deficit on the ODR task depended on
the dose of injected drug; higher doses of
SCH23390 produced larger increases in errors of the memory-guided saccades (Fig.
4B).
Although SCH23390 is a selective antagonist of D1 receptors, it also appears to bindto serotonin (5-HT2) receptors (19) and it
might be argued that the effect of
SCH23390 was due to effects at 5-HT2
receptors. We therefore examined the effects
of a selective antagonist of the 5-HT2 receptor, ketanserin, and an inactive analog of
SCH23390, SCH23388, on ODR performance in two monkeys. Local injection of
ketanserin (100 ptg, five sites) or SCH23388(100 pug, four sites) near the same sites atwhich the injection of SCH23390 induced
A
0

8 0

+

6

a

2

_

000

c)

6-

6

40

60

80

0

-20

0

20

0

60

8

0

20

40

60

80

D

SCH39166

0060Mg
0 30 Mg

+

io
1020

20

ca c

0

8

A.-4
0

0

120

A1.5ss6-.aSCH2339016
14

0 3.0 s

0

A'

-:-20
so

>

B
0 6.0 s049SCH23390 failed to induce any significant
changes in performance on either the ODRor the control task. Thus, the effect of
SCH23390 does not appear to be a consequence of its nonspecific effects or any effecton 5-HT2 receptors.
We further tested the pharmacological
specificity of the effect by injecting
SCH39166 into two of the three monkeys.
Unlike SCH23390, this Dl antagonist has anegligible affinity for 5HT-2 receptors (12).
When we injected SCH39166 (1 to 10 Kig)
into seven sites in the principal sulcal region(Table 1 and Fig. 1), the injection induced
deficits in performance in the ODR task but
not in the control task. The impairment was
similar to that induced by SCH23390: after
the injection of SCH39166, the error andonset latency of memory-guided saccades

SCH23390

10^

deficits in the ODR task did not produce
any clear changes in performance on either
the ODR or the control task. In addition,
the injection of 0.9% saline (5 to 10 pl) into
sites that were associated with deficits in
ODR performance after injection of

0

20o

0

0 5 s-ODR* 2 -ODR
A CON

+

15
10
o,

0

-20

-

--0

--I
- - -

0 ..4.. 60
0
40
20
60

8

80

0

-20

0

.
20

40

60

80

Time after Injection (min)Fig. 4. (A) The effect of SCH23390 on the ODR at different delay lengths. SCH23390 (30 pug) was
injected into the left PFC while the monkey performed the ODR task with different durations of delay(site 2 in Table 1). The data are for trials at the location indicated by the arrow (inset), since thememory-guided saccade to this target location was the most strongly affected by the injection. Mean ±SEM; n = 4 to 8 trials per time point. (B) The effect of SCH23390 on the ODR at different doses.
SCH23390 was injected into the same sites in the left PFC in different daily sessions (site 3 in Table 1).
The injection sites were near the site of the case shown in (A). The data are for trials at the location
indicated by the arrow (inset); the memory-guided saccade to this target location was the most strongly
affected by the injection. Mean ± SEM; n = 4 to 8 trials per time point. (C) The effect of the DI
antagonist SCH39166 on the ODR and CON tasks. SCH39166 (5 ,ug) was injected into the right PFC
while the monkey performed the ODR task with 2- or 5-s delays and the CON task with a 5-s delay (site
24 in Table 1). The data are for trials at the lower-left target location (inset); the memory-guided
saccade to this target location was the most severely impaired. Mean + SEM; i = 4 to 9 trials per time
point. (D) The effect of the D2 antagonist raclopride on the ODR and CON task. Raclopride (100 plg)
was injected into the same site as that of the case shown in (C). The data are for trials at the lower-lefttarget location (inset). Mean + SEM; n = 4 to 6 trials per time point. No significant changes indiscrepancies or onset latencies were observed after the injection for any task. However, comparisons of
discrepancies and latencies revealed a significant difference between the ODR and CON tasks for almost
all time periods. This difference existed before drug injection as well as after and reflects the greaterdifficulty of the ODR compared to the CON task.
22 FEBRUARY 1991

REFERENCES AND NOTES

1. P. S. Goldman-Rakic, in Handbook of Pitysiolsy,

Raclopride

25

25

to

were increased for a few specific target locations, and the deficits were sensitive to theduration of delay (Fig. 4C). Furthermore,
we injected SCH39166 into four sites thatwere associated with deficits after
SCH23390 injection and obtained the same
results as those independently obtained with
SCH23390. In contrast, injection of 0.9%
saline (5 to 7 Al) into these same sites andothers in which SCH39166 caused deficits
did not affect either the ODR or the control
task performance. Moreover, we also examined the effects of injecting the selective D2
receptor antagonist raclopride (20) (100pg) into seven sites associated with deficits
produced by SCH39166 or SCH23390;
raclopride did not affect the ODR or thecontrol task performance (Fig. 4D).
Our findings indicate that the activationof D1 receptors is critical for the memory
processes mediated by the primate PFC.
They do not, however, rule out possibleroles for receptors other than D1 or interactions between D 1 receptors and other receptors in the mnemonic function of the PFC.
Also, our results do not indicate the specific
type of neuron that is affected by D 1 receptor antagonism (21). However, cells or processes with D 1 receptors are heavily concentrated in the deep layers of the PFC, where
neurons that project to the thalamus, caudate nucleus, and superior colliculus arelocated (4, 22). Disruption of neuronal activity of one or more of these cell classes may
be responsible for the mnemonic deficit.

Section 1: The Nervous Systemn, vol. 5, Hiiher Fitiictions of the Brain, part 1, F. Plum, Ed. (Oxford Univ.
Press, New York, 1987). p. 373.
2. R. M. Brown, A. M. Crane, P. S. Goldman, Brain
Res. 168, 133 (1979).
3. B. Berger, S. Trottier, C. Vernev, P. Gaspar, P. C.
Alvarcz, J. (omnp. Neurol. 273, 99 (1988); P.
Gaspar, B. Berger, A. Febvret, A. Vignv, J. P.
Henrv, ibid. 279, 249 (1989); P. Levitt, R. Rakic,
P. S. Goldman-Rakie, ibid. 225, 1 (1984); D. A.
Lewis, M. J. Campbell, S. L. Foote, M. Goldstein, J.
H. Morrison, J. Neurosci. 7, 279 (1987); 1). A.
Lewis, S. L. Foote, M. Goldstein, J. H. Morrison,
Brain Res. 449, 225 (1988).
4. P. S. Goldman-Rakic, M. S. Lidow, D. W. Gallager,
J. Neurosci. 10, 2125 (1990); M. S. Lidow, P. S.
Goldman-Rakic, P. Rakic, R. B. Innis, Proc. Nati.
Acad. Sci. U.S.A. 86, 6412 (1989).
5. T. J. Brozoski, R. M. Brown, H. E. Rosvold, P. S.
Goldman, Scienice 205, 929 (1979).
6. T. Sawaguchi, M. Matsumura, K. Kutx)ta, Neurosci.
Res. 5, 465 (1988); J. Neurophysiol. 63, 1385
(1990).
7. J. W. Kebabian and 1). B. Calne, Nature 277, 93(1979); M. Memo, C. Missale, M. 0. Carruba, P. F.
Spano, J. Neural Transpn. Suppl. 22, 19 (1986).
8. R. Cortes, B. Gueve, A. Pazos, A. Probs, J. M.

Palacios, Neurosciena 28, 263 (1989).

9. L. Farde, C. Halldin, S. Stone-Elander, G. Sedvall,
Psychophartnacolo.y 92, 278 (1987); E. K. Richfield,
A. B. Yong, J. B. Penney, J. Comnp. Neurol. 286,
409 (1989); H. Hall, L. Farde, G. Sedvall, J. Neural

Tratis-n. 73, 7 (1988).

10. M. Camps, R. Cortes, B. Gueye, A. Probs, J. M.
Palacios, Neuroscience 28, 275 (1989); L. Farde etal. Psychopharnnacology 94, 471 (1988).
REPORTS

949

11. J. W. Kebabian et al., Trends Pharinacol. Sci. 7, 96(1986).
12. R. E. Chipkin, L. C. Irio, V. L. Coffin, R. D.
McQuadc, J. G. Berger, A. Barnett,J. Phartnacol.
Exp. Ther. 247, 1093 (1988).
13. S. Funahashi, C. J. Bruce, P. S. Goldman-Rakic,
J. Neurophysiol. 61, 331 (1989).
14. _ _, Soc. Neurosci. Abstr. 12, 554 (1986).
15. In the ODR task, the monkeys fixated a central spot
on a cathode-ray tube, and a visual cue came on for
0.3 s, followed by a delay period. The cue waspresented randomly at one of several peripheral
locations (n = 6 to 22, usually six locations), whichwere separated by 45' or 90' and whose eccentricities were 7° to 20' (usually 20'). After the delay
period (1.5 to 6 s, but usually 5 s), the fixation spot
was then extinguished, which instructed the monkeys to make a memory-guided saccade to thelocation that had been cued before the delay period.
The correct response was rewarded by a drop ofjuice 0.2 s after the response. Trials were separated
by an intertrial interval of 3.5 s. The control task wasexactly the same as the ODR task except that thetarget remained on during the "delay" period, thus
providing sensory guidance for saccade in the response period.

16. A micromanipulator on a cylinder mounting on theskull was used to insert the syringe into the cortex
and to control it precise localization and relocalization in subsequent sessions. The spread of 3 p.1 of
injected solution into the cerebral tissue is about 3
mm in diameter [R. D. Myers, Psychol. Bchav. 1,
171 (1966)].
17. The experimental sessions consisted of blocks oftrials with a time length of 5 or 10 min. In eachblock, the monkey performed the ODR or control(CON) task, and the blocks associated with the
CON task were intermixed with the blocks associated with the ODR task in most cases. The monkeys
performed two to four CON and two to four ODR
blocks before and at least four blocks of each task
after the injection. The following behavioral parameters were examined: discrepancy between the target
location and the end point of the saccade during the
response period; the onset latency of the response
after the onset of the go signal; trajectories ofsaccades; and amplitude and velocity of saccades.
Velocity was measured from the amplitude andduration of the saccades. The predrug blocks werecombined into one score for each task, and thispredrug block was compared with every postdrug
block by a one-way analysis of variance followed by__ 11 UPIRIForm, Motion, and Binocular Rivalry
If one looks at two grossly dissimilar
images-such as orthogonal gratingsthrough a stereo viewer, only one eye's fieldofvision is seen at a time. This phenomenon
is called binocular rivalry (1). N. K. Logothetis and J. D. Schall (2) performed aningenious experiment to explore the neuralbasis of binocular rivalry. A monkey looked
at a downward-moving "conveyor belt" ofhorizontal stripes through one eye and at
upward-moving horizontal stripes throughthe other eye. While the monkey "reported"
rivalry by pressing the appropriate key, theelectrical activity of direction-selective neurons in the middle temporal (MT) area inthe superior temporal sulcus was monitored.
One might suppose that neural responses
corresponding to the suppressed image
would be silenced while neurons corresponding to the other image would be active. Although 10% of the cells showed the
expected suppression, in most neurons nosimple suppression was observed-certainly
nothing similar to the complete occlusionthat occurs perceptually. Indeed, sometimes
there was an enhancement of neural responses to the suppressed image.
One possible explanation for this neuronal response would be that rivalry is a
"network" property that cannot be studiedin single cells, but this statement is notuseful, even if it were true. A second explanation would be that rivalry is not a complete occlusion of one eye's input at an earlystage, rather, it occurs at multiple sites and950

can selectively involve some neural channels
while sparing others (3, 4). For example,
stereopsis can be experienced in the presenceof "form rivalry" (4, 5) even though only
one image is perceived at a time. In the caseof downward-moving stripes for the left eye
and upward for the right eye, it is true that
only one image is seen at a time, but is thisreally "motion rivalry" caused by inhibition
between motion channels within the MTarea itself? Even though the stripes arehorizontal for both eyes, at any given instantthe stripes are likely to be vertically misaligned. This would tend to generate form
rivalry by stimulating noncorresponding retinal points (5). Perhaps it is this form rivalry
that gates neural motion signals (6)-there
may be no motion rivalry per se occurring
within the MT.
I did an experiment recently (6) to study
these effects. After I viewed the "conveyor
belt" display for several minutes, two motion after-effects were generated. On looking at the world with the right eye I perceived downward movement, and on
looking with the left eye I perceived upward
motion. What happened when I opened
both eyes depended on what I looked at. A
stationary grating (or any pattern) usuallylooked stationary-the brain simpy averaged the motion after-effects from both eyes.
But on presenting diagonal, orthogonal, stationary gratings to both eyes-so that I
experienced form rivalry-I experienced
motion rivalry as well! The left eye perceived

the Newman-Keuls procedure for multiple comparisons. The data in Table 1 are for injections in which
at least one ODR postdrug block differed significantly from the predrug block.
18. Bradykinesia (slowing of responses) is characteristicof Parkinson's disease, a disease in which DA loss inthe neostriatum is the cardinal pathognomonic finding. Our result of an increased latency to respond in
the ODR task indicates that slowing of at least somememory-guided responses might be attributable tocortical DA dysfunction.
19. S. Bischoff, M. Heinrich, J. M. Sountag, J. Krauss,Eur. J. Pharinacol. 129, 367 (1986).
20. C. Kohler, H. Hall, S.-O. Orgen, L. Gawell, Biochern. Phartnacol. 34, 2251 (1985).
21. Funahashi et al. (13) have recently identified at least
five different types of neuronal processes associatedwith ODR performance, and D 1 receptors might beselectively associated with only one or a subset ofthese.
22. B. Berger, P. Greengard, P. S. Goldman-Rakic, Soc.
Neturosci. Abstr. 15, 428 (1989).
23. Supported by National Institute of Mental Healthgrants MH44866 and MH38546.
16 July 1990; accepted 31 October 1990

upward motion and the right eye perceived
downward motion.
I conclude that the motion signals fromthe two eyes were averaged only when I
looked at the same form with both eyes. If
there was form rivalry, on the other hand,
the motion signals inhibit each other. Apparently, what happened in the form channels influenced what happened in the motion channels. Since the MT area isconcerned with motion rather than form,
these results may explain why Logothetis etaA. did not observe a simple suppression of
one eye's motion signals. Indeed, our results
suggest that the best place to look for rivalry
would be in the "form area" DL, V4, or IT
rather than in MT. The presence of rivalry inthese areas might modulate the activity ofcells in the MT area in complex ways orinteract with cells in higher motion areas
such as the medial superior temporal arearather than in the MT itself.
A third explanation would be in terms ofthe theory of F. H. C. Crick and C. Koch(7), according to which the basis ofconscious
visual awareness is the synchronization of
40HTZ oscillations (8). If one is aware of an
object, the firing of all neurons that are simultaneously activated by that object alone becomes synchronized. This synchronization
does not include other neurons that are activated by objects that one is not attending to.
A reanalysis of the data of Logothetis and
Schall to look for synchronized oscillations(rather than suppression) may therefore be
worthwhile. Such data could provide a test
for the hypothesis that synchronized oscillations are actually involved in consciousness
and not merely in binding features together
for object segmentation.
V. S. RAMACHANDRAN
Department of Psychology and
SCIENCE, VOL. 251