Separate, Causal Roles of the Caudate
in Saccadic Choice and Execution
in a Perceptual Decision Task
Long Ding1,* and Joshua I. Gold1
1Department of Neuroscience, University of Pennsylvania, Philadelphia, PA 19104, USA
In contrast to the well-established roles of the stria-
tum in movement generation and value-based deci-
sions, its contributions to perceptual decisions lack
direct experimental support. Here, we show that
electrical microstimulation in the monkey caudate
nucleus influences both choice and saccade re-
sponse time on a visual motion discrimination task.
Within a drift-diffusion framework, these effects
consist of two components. The perceptual compo-
nent biases choices toward ipsilateral targets, away
from the neurons’ predominantly contralateral re-
sponse fields. The choice bias is consistent with
a nonzero starting value of the diffusion process,
which increases and decreases decision times for
contralateral and ipsilateral choices, respectively.
The nonperceptual component decreases and in-
creases nondecision times toward contralateral and
ipsilateral targets, respectively, consistent with the
caudate’s role in saccade generation. The results
sions used to select saccades that may be distinct
from its role in executing those saccades.
The basal ganglia have been known for more than a century to
play important roles in movement control (Ferrier, 1873; Wilson,
functions, including various forms of decision making, have also
become better appreciated (Brown et al., 1997; Divac et al.,
1967; Middleton and Strick, 2000). For example, the basal
ganglia havebeen causallylinked toreward-modulated behavior
and represent a key component in value-based decision making
(Barto, 1995; Cai et al., 2011; Hikosaka et al., 2006; Hollerman
et al., 2000; Kable and Glimcher, 2009; Samejima and Doya,
2007). It is unclear if and how the basal ganglia also contribute
to perceptual decisions that link sensory input to oculomotor
Support for the basal ganglia’s role in perceptual decision
making comes from several sources. The basal ganglia receive
diverse anatomical inputs from almost all parts of sensory and
sensory-motor cortical areas (Figure 1A). These areas include
the middle temporal (MT) and medial superior temporal (MST)
areas of extrastriate cortex, lateral intraparietal cortex (LIP),
and parts of prefrontal cortex including the frontal eye field
(FEF) (Maunsell and van Essen, 1983; Saint-Cyr et al., 1990; Se-
lemon and Goldman-Rakic, 1985, 1988; Yeterian and Pandya,
1995), all with well-characterized activity related to a task linking
a decision about visual motion to saccadic eye movements (Brit-
ten et al., 1992, 1996; Ding and Gold, 2012; Ditterich et al., 2003;
Hanks et al., 2006; Kim and Shadlen, 1999; Newsome et al.,
1989;Roitman andShadlen, 2002;Salzmanetal.,1992;Shadlen
and Newsome, 1996). Theoretical studies have ascribed several
decision-related computations to specific components of the
basal ganglia (Berns and Sejnowski, 1995; Bogacz and Gurney,
2007; Lo and Wang, 2006; Rao, 2010). Single-unit activity in the
encode a number of decision-related signals in monkeys per-
forming the visual motion saccade task (Ding and Gold, 2010).
fMRI studies revealed striatal activation in human subjects per-
forming visual motion discrimination tasks (Forstmann et al.,
2008; van Veen et al., 2008). In contrast, the frequency of clini-
cally observed perceptual impairments is much lower than that
of motor deficits for diseases associated with basal ganglia
dysfunction (e.g., Parkinson’s disease). This observation seems
to argue against a major role of the basal ganglia in perceptual
decision-making, although non-motor symptoms are often
under-reported or unrecognized by clinicians (Chaudhuri et al.,
In this study, we used electrical microstimulation in the
caudate nucleus in monkeys performing a visual motion discrim-
ination task (Figure 1) to address three questions: (1) is there
a causal link between caudate activity and perceptual decision
behavior? (2) What are the specific decision-related computa-
tions that are influenced by caudate activity? (3) How do the
basal ganglia’s roles in perceptual decisions relate to their roles
in movement control? The results indicate that the basal ganglia
can bias perceptual decisions toward particular alternatives.
These effects are distinct from their role in movement execution.
Thus, the basal ganglia appear to make multiple causal contri-
butions to simple decisions that link sensory input to motor
Neuron 75, 865–874, September 6, 2012 ª2012 Elsevier Inc. 865
Microstimulation Did Not Alter the Monkeys’ Task
As described in previous reports (Ding and Gold, 2010, 2012),
the performance of the two monkeys on the RT dots task de-
pended critically on the strength (coherence) of the motion stim-
ulus. Bothmonkeysachieved near-perfect accuracyandhadthe
shortest RTs for coherences >20%, with steadily decreasing
accuracy and increasing RT at lower coherences (Figure 2).
We fit choice and RT performance simultaneously with a drift-
diffusion model (DDM; see Experimental Procedures and curves
in Figure 2), and we fit choice data alone using logistic functions
(see Figure S2 available online). We quantified performance
using two measures estimated from the fits: choice bias, corre-
sponding to the horizontal position of the psychometric curve
(Figure 2, top panels), and discrimination threshold, correspond-
ing to the steepness of the psychometric curve.
We examined the effects of electrical microstimulation on
performance in 43 sessions (n = 29 and 14, for monkey C and
F, respectively). The microstimulation sites were within the
general regions sampled in our previous recording study (Fig-
ure S1; Ding and Gold, 2010). The motion directions used were
similar to our previous recoding studies for the caudate nucleus
and FEF (Table S1; Ding and Gold, 2010, 2012). The inclusion of
randomly interleaved microstimulation trials did not appear to
affect the monkeys’ overall strategy for solving the task. For
example, when comparing performance on trials without micro-
stimulation from this study to performance of the same monkeys
on the same task in a recent study in which no microstimulation
was used (Ding and Gold, 2012), choice bias and discrimination
threshold were not significantly different for both monkeys and
for all motion axes tested (Wilcoxon rank-sum test, p > 0.05).
Moreover, the DDM fit separately to trials with and without mi-
crostimulation in this study had comparable goodness of fits
(Wilcoxon signed-rank test for H0: equal log-likelihood, p = 0.14).
Microstimulation Influenced Choice and RT
The effects of caudate microstimulation on performance are
shown for two representative sessions in Figure 2. In both cases,
microstimulation caused the monkeys to favor the T1 choice
(ipsilateral to the microstimulation sites), reflected in a leftward
shift of the psychometric function (top panels). The T1 choices
reflected in a downward shift in the chronometric function for
positive coherence values (bottom panels). Using the DDM fit
simultaneously to psychometric and chronometric data, the
change in bias when comparing trials with and without micro-
stimulation (Dbias; positive/negative values imply more T2/T1
choices on microstimulation trials) was ?4.2% and ?5.0%
coherence for monkeys C and F, respectively, for these sessions
(bootstrap methods, p < 0.05 for both). In contrast, Dthreshold
(positive/negative values imply higher/lower threshold on micro-
stimulation trials) was ?1.1% and 2.2% coherence, respectively
(bootstrap methods, p > 0.05 for both).
Across sessions, electrical microstimulation had a consistent
effect on choice biases, inconsistent effects on thresholds, and
mixed effects on RTs (Figure 3). A significant Dbias was
observed in 18 out of 29 and 7 out of 14 sessions for monkeys
Cand F,respectively(we defined asignificant effectasa session
in which the value measured on trials with microstimulation fell
using bootstrapping from trials without microstimulation). More-
over, Dbias tended to be negative, representing an increased
preference for ipsilateral or upward choices (Figure 3A; mean
Dbias = ?2.7% coherence, t test for H0: mean = 0, p < 0.0001).
Incontrast, asignificant Dthreshold wasobserved inonly8and1
sessions for monkeys C and F, respectively, with a mean value
across all sessions that did not differ significantly from zero (Fig-
ure 3B; mean = 0.2% coherence; p = 0.47). For sessions with
significant nonzero Dbias, the mean RT for correct, microstimu-
lation-favored choices was shorter on microstimulation trials
(Wilcoxon signed-rank test, p = 0.0026), an effect that was larger
for lower coherences (Figure 3C, circles). The mean RT for
correct, other choices was not different between microstimula-
tion conditions (p = 0.37; Figure 3C, triangles). For other ses-
sions, RT was not significantly affected for either choice (p =
0.41 and 0.15 for T1 and T2 choices, respectively).
The observed Dbias was robust and independent of our
choice of fitting with a DDM. Using logistic-only psychometric
Figure 1. Simplified Oculomotor System
Diagram and the Behavioral Task
(A) A schematic drawing illustrating the major
connections of the oculomotor basal ganglia for
temporal visual area; LIP, lateral intraparietal
cortex; FEF, frontal eye field; GPe, external
segment of the globus pallidus; STN, subthalamic
nucleus; SNr, substantia nigra pars reticulata; SC,
superior colliculus; DA, dopamine.
(B) Behavioral task. The monkey decides the
direction of random-dot motion and then re-
sponds, at a self-determined time, by making
a saccade to foveate one of two choice targets.
Saccades to the target in the direction of coherent
motion (assigned randomly for 0% coherence)
are followed by juice reward. Electrical micro-
stimulation is delivered during motion viewing and
terminated when the monkey makes a saccade.
Caudate Stimulation Biases Perceptual Decisions
866 Neuron 75, 865–874, September 6, 2012 ª2012 Elsevier Inc.
Hikosaka, O., Sakamoto, M., and Usui, S. (1989). Functional properties of
monkey caudate neurons. I. Activities related to saccadic eye movements.
J. Neurophysiol. 61, 780–798.
Hikosaka, O., Sakamoto, M., and Miyashita, N. (1993). Effects of caudate
nucleus stimulation on substantia nigra cell activity in monkey. Exp. Brain
Res. 95, 457–472.
Hikosaka, O., Nakamura, K., and Nakahara, H. (2006). Basal ganglia orient
eyes to reward. J. Neurophysiol. 95, 567–584.
Hollerman, J.R., Tremblay, L., and Schultz, W. (2000). Involvement of basal
ganglia and orbitofrontal cortex in goal-directed behavior. Prog. Brain Res.
Horwitz, G.D., and Newsome, W.T. (1999). Separate signals for target selec-
tion and movement specification in the superior colliculus. Science 284,
Kable, J.W., and Glimcher, P.W. (2009). The neurobiology of decision:
consensus and controversy. Neuron 63, 733–745.
Kim, J.N., and Shadlen, M.N. (1999). Neural correlates of a decision in the
dorsolateral prefrontal cortex of the macaque. Nat. Neurosci. 2, 176–185.
Kitama, T., Ohno, T., Tanaka, M., Tsubokawa, H., and Yoshida, K. (1991).
Stimulation of the caudate nucleus induces contraversive saccadic eye move-
ments as well as head turning in the cat. Neurosci. Res. 12, 287–292.
function: a commentary. Percept. Psychophys. 63, 1421–1455.
Kravitz, A.V., Freeze, B.S., Parker, P.R., Kay, K., Thwin, M.T., Deisseroth, K.,
and Kreitzer, A.C. (2010). Regulation of parkinsonian motor behaviours by op-
togenetic control of basal ganglia circuitry. Nature 466, 622–626.
Kravitz, A.V., Tye, L.D., and Kreitzer, A.C. (2012). Distinct roles for direct and
indirect pathway striatal neurons in reinforcement. Nat. Neurosci. Published
online: April 29, 2012. http://dx.doi.org/10.1038/nn.3100.
Law, C.T., and Gold, J.I. (2008). Neural correlates of perceptual learning in
a sensory-motor, but not a sensory, cortical area. Nat. Neurosci. 11, 505–513.
Lo, C.C., and Wang, X.J. (2006). Cortico-basal ganglia circuit mechanism for
a decision threshold in reaction time tasks. Nat. Neurosci. 9, 956–963.
Maunsell, J.H., and van Essen, D.C. (1983). The connections of the middle
temporal visual area (MT) and their relationship to a cortical hierarchy in the
macaque monkey. J. Neurosci. 3, 2563–2586.
Middleton, F.A., and Strick, P.L. (2000). Basal ganglia output and cognition:
evidence from anatomical, behavioral, and clinical studies. Brain Cogn. 42,
Nakamura, K., and Hikosaka, O. (2006a). Facilitation of saccadic eye move-
ments by postsaccadic electrical stimulation in the primate caudate.
J. Neurosci. 26, 12885–12895.
Nakamura, K., and Hikosaka, O. (2006b). Role of dopamine in the primate
caudate nucleus in reward modulation of saccades. J. Neurosci. 26, 5360–
Newsome, W.T., Britten, K.H., and Movshon, J.A. (1989). Neuronal correlates
of a perceptual decision. Nature 341, 52–54.
Niijima, K., and Yoshida, M. (1982). Electrophysiological evidence for branch-
ing nigral projections to pontine reticular formation, superior colliculus and
thalamus. Brain Res. 239, 279–282.
on the speed and accuracy of a perceptual decision. J. Vis. 5, 376–404.
Parent, A., and Hazrati, L.N. (1995). Functional anatomy of the basal ganglia. I.
The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev.
Petrov, A.A., Van Horn, N.M., and Ratcliff, R. (2011). Dissociable perceptual-
learning mechanisms revealed by diffusion-model analysis. Psychon. Bull.
Rev. 18, 490–497.
Rao, R.P. (2010). Decision making under uncertainty: a neural model
based on partially observable markov decision processes. Front. Comput.
Neurosci. 4, 146.
Ratcliff, R. (1978). Theory of memory retrieval. Psychol. Rev. 85, 59–108.
Roitman, J.D., and Shadlen, M.N. (2002). Response of neurons in the lateral
intraparietal area during a combined visual discrimination reaction time task.
J. Neurosci. 22, 9475–9489.
Saint-Cyr, J.A., Ungerleider, L.G., and Desimone, R. (1990). Organization of
visual cortical inputs to the striatum and subsequent outputs to the pallido-
nigral complex in the monkey. J. Comp. Neurol. 298, 129–156.
Salzman, C.D., Murasugi, C.M., Britten, K.H., and Newsome, W.T. (1992).
Microstimulation in visual area MT: effects on direction discrimination perfor-
mance. J. Neurosci. 12, 2331–2355.
Samejima, K., and Doya, K. (2007). Multiple representations of belief states
and action values in corticobasal ganglia loops. Ann. N Y Acad. Sci. 1104,
Selemon, L.D., and Goldman-Rakic, P.S. (1985). Longitudinal topography and
interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci.
Selemon, L.D., and Goldman-Rakic, P.S. (1988). Common cortical and
subcortical targets of the dorsolateral prefrontal and posterior parietal cortices
in the rhesus monkey: evidence for a distributed neural network subserving
spatially guided behavior. J. Neurosci. 8, 4049–4068.
Shadlen, M.N., and Newsome, W.T. (1996). Motion perception: seeing and
deciding. Proc. Natl. Acad. Sci. USA 93, 628–633.
Shen, W., Tian, X., Day, M., Ulrich, S., Tkatch, T., Nathanson, N.M., and
Surmeier, D.J. (2007). Cholinergic modulation of Kir2 channels selectively
elevates dendritic excitability in striatopallidal neurons. Nat. Neurosci. 10,
Smith, P.L., and Vickers, D. (1988). The accumulator model of 2-choice
discrimination. J. Math. Psychol. 32, 135–168.
Spatz, W.B., and Tigges, J. (1972). Experimental-anatomical studies on the
‘‘middle temporal visual area (MT)’’ in primates. I. Efferent cortico-cortical
connections in the marmoset Callithrix jacchus. J. Comp. Neurol. 146,
responses. J. Neurosci. Methods 65, 1–17.
Tomasi, S., Caminiti, R., and Innocenti, G.M. (2012). Areal differences in diam-
eter and length of corticofugal projections. Cereb. Cortex 22, 1463–1472.
van Veen, V., Krug, M.K., and Carter, C.S. (2008). The neural and computa-
tional basis of controlled speed-accuracy tradeoff during task performance.
J. Cogn. Neurosci. 20, 1952–1965.
Watanabe, M., and Munoz, D.P. (2010). Saccade suppression by electrical
microstimulation in monkey caudate nucleus. J. Neurosci. 30, 2700–2709.
Watanabe,M., and Munoz, D.P. (2011). Saccadereaction times are influenced
bycaudatemicrostimulation following andpriortovisualstimulusappearance.
J. Cogn. Neurosci. 23, 1794–1807.
Williams, Z.M., and Eskandar, E.N. (2006). Selective enhancement of associa-
tive learning by microstimulation of the anterior caudate. Nat. Neurosci. 9,
Wilson, S.A.K. (1914). An experimental research into the anatomy and physi-
ology of the corpus striatum. Brain 36, 427–492.
Yeterian, E.H., and Pandya, D.N. (1995). Corticostriatal connections of extras-
triate visual areas in rhesus monkeys. J. Comp. Neurol. 352, 436–457.
Caudate Stimulation Biases Perceptual Decisions
874 Neuron 75, 865–874, September 6, 2012 ª2012 Elsevier Inc.