*Laboratory for Integrative
Institute on Alcohol Abuse
and Alcoholism, National
Institutes of Health, 5625
Fishers Lane, TS-13,
Bethesda, Maryland 20892,
USA. ‡Department of
Psychology, Franz Hall,
University of California, Los
Correspondence to B.J.K.
The role of the basal ganglia in habit
Henry H. Yin* and Barbara J. Knowlton‡
Abstract | Many organisms, especially humans, are characterized by their capacity for
intentional, goal-directed actions. However, similar behaviours often proceed
automatically, as habitual responses to antecedent stimuli. How are goal-directed actions
transformed into habitual responses? Recent work combining modern behavioural assays
and neurobiological analysis of the basal ganglia has begun to yield insights into the neural
basis of habit formation.
When you flip on a light switch, your behaviour could be
a result of the desire for a state of illumination coupled
with the belief that a certain movement will lead to it.
Sometimes, however, you just turn on the light habitu-
ally, without anticipating the consequences — the very
context of having arrived home in a dark room auto-
matically triggers your reaching for the light switch.
Although to the observer these two cases might appear
to be similar, they differ in the extent to which they
are controlled by outcome expectancy. When the light
switch is known to be broken, the habit might still persist
whereas the goal-directed action might not.
Intuitively, then, goal-directed actions are control-
led by their consequences, habits by antecedent stimuli.
But how can we translate such intuitive concepts into
operationally defined terms and experimentally test-
able hypotheses? Here, we outline the basic conceptual
framework that has emerged from the behavioural
analysis of goal-directed actions and stimulus-driven
habits, and integrate this framework with recent find-
ings on the anatomy and physiology of the basal ganglia,
a set of nuclei that have long been known to control
voluntary behaviour. More specifically, we show that
distinct networks involving the basal ganglia are the
neural implementations of actions and habits, and that
an understanding of these networks can illuminate find-
ings from different levels of analysis, from the cellular
and molecular mechanisms of synaptic plasticity to the
conditions that favour habit formation and the develop-
ment of compulsivity in various clinical disorders.
Basal ganglia and instrumental behaviours
The basal ganglia: anatomy and functions. The basal
ganglia are a set of nuclei located in the cerebrum (FIG. 1).
Unlike the cortex, which has excitatory, glutamatergic
projection neurons, the basal ganglia contain inhibitory,
GABA (γ-aminobutyric acid)-containing projection
neurons. Of these projection neurons, the spiny variety
belongs to the striatum (the input nucleus) and the aspiny
variety belongs to the pallidum (the output nucleus)1,2.
The striatal projection neurons are often quiescent
owing to their intrinsic membrane properties2, and when
they are activated by strong and coherent inputs from the
cortex (and, to a lesser extent, the thalamus), they tend to
reduce the tonically active pallidal output. The outcome
of this disinhibitory pathway, the most basic pathway
in the basal ganglia, is the facilitation of the targeted
motor network3. However, a different pathway, tradi-
tionally known as the ‘indirect pathway’, appears to exert
inhibitory control over downstream thalamocortical
and brainstem networks4.
In discussing the role of the basal ganglia in behav-
iour, it is useful to think of them as a biological system
that operates by classic selectionist principles, possess-
ing a generator of diversity and mechanisms of selection
and of differential amplification. The striatum receives
massive projections from almost all cortical areas, and
from the intralaminar nuclei of the thalamus. These are
organized roughly by the area from which the projection
arises. The thalamocortical network, which projects to
the striatum, provides a wealth of inputs that represent
a diverse array of signals related to representations
of sensory inputs, motor programmes and internal
states2,5. This dynamic set of inputs, which can change
from moment to moment, therefore constitutes a gen-
erator of diversity. Moreover, the basal ganglia, and in
particular the striatum, are capable of selection and dif-
ferential amplification: in the short term through lateral
inhibition and the membrane properties of the striatal
projection neurons, which shift between different states
464 | JUNE 2006 | VOLUME 7
of excitability; and in the long run by long-term synap-
tic plasticity, which can preserve or alter the process of
Instrumental behaviour. Given their crucial place in
the cerebrum, how do the basal ganglia function in
generating purposive behaviour? Divac7 and Konorski8
were among the first to systematically examine the
effects of cortical and basal ganglia lesions on the
acquisition of instrumental behaviours. Whenever
a particular outcome is contingent on a response,
be it flexing a leg, traversing a maze or pressing a
lever, the behaviour in question is instrumental.
Instrumental behaviours differ from reflexes and
fixed action patterns, which are not controlled by the
contingency between behaviour and its consequences.
Lesions of the sensorimotor cortex severely impaired
skilled movements, and lesions of the premotor
cortex impaired the chaining of action repertoires.
By contrast, lesions of the basal ganglia (particularly
the striatum) disrupted the very ‘instrumentality’ of
actions — despite relatively intact fine movements,
the animals that were tested could no longer perform
or acquire actions in order to earn specific rewards or
avoid aversive stimuli8.
Although Konorski8 presciently observed that striatal
lesions produced variable results, he did not have at his
disposal behavioural assays that would have allowed him
to precisely analyse these effects. A major obstacle to
understanding basal ganglia function is the conceptual
confusion that characterized the field of instrumental
learning for many decades, which in some ways persists
even today. Although instrumental behaviour appears to
be primarily directed towards a goal, traditional theories,
with a few notable exceptions9,10, dismissed this obvious
possibility. In the prime of behaviourism research, the
study of learning was dominated by Hull and his fol-
lowers, for whom instrumental learning is described in
terms of stimulus–response (S–R) bonds strengthened
by subsequent reinforcement11,12. S–R/reinforcement
theory was based on the work of Thorndike, and aimed
to eliminate ‘unscientific’ concepts such as intentional-
ity, expectancy and internal representation11,12. The
most fundamental assumption of this theory is that all
behaviour is elicited by some antecedent stimuli from
the external environment, and that the consequences of
behaviour, by providing satisfaction or dissatisfaction to
the organism, merely reinforces or weakens the S–R asso-
ciation. Deliberately dismissing the intentional account
of goal-directed behaviour — that our behaviour can
be controlled by action–outcome contingencies — the
S–R/reinforcement theorist assigned no causal role to
outcome expectancy. Although this position might be
considered extreme today, its pervasive influence on
neuroscience can hardly be exaggerated, and it remains
powerful in many of the implicit assumptions made by
researchers who interpret all neural activity solely as
a function of antecedent stimuli presented before the
However, research over the past two decades has
shown conclusively that animals can encode the causal
relationship between their actions and outcomes, and
control their actions according to their anticipation of,
and desire for, the outcome13,14. Consequently, we are
now aware of the paramount importance of two previ-
ously neglected variables — the remembered value of
the expected outcome and the knowledge of the causal
relationship between the action and the outcome. The
realization that these variables can be manipulated by the
experimenter has revolutionized the study of purposive
As a result of this paradigm shift, there are now
experimental assays that measure intentionality and
goal-directedness. Two classes of assay have become
common in the contemporary analysis of instrumental
learning. In the first, the value of the outcome is increased
(inflated) or decreased (devalued). Devaluation is far
more common because it is easier to reduce the value of
an outcome; for example, by giving the animal unlim-
ited exposure to the food reinforcer before a brief probe
test. If performance is sensitive to manipulations of
outcome value (for example, if the rate of responding
decreases after outcome devaluation), then the behav-
iour is controlled by the anticipation of the outcome. If
performance is insensitive to these manipulations, then
the behaviour is controlled by antecedent stimuli (it
is habitual). Importantly, this test should occur in the
absence of the outcome to probe the nature of memory
for the association independently of new learning that
can occur during the test.
In the second class of assays, the action–outcome
contingency (A–O; the degree to which the outcome
depends on the action) is manipulated14,15. This is often
Figure 1 | A schematic of the main connections of the
basal ganglia. Simplified illustration of basal ganglia
anatomy based on a primate brain. The direct and indirect
pathways from the striatum have net effects of
disinhibition and inhibition on the cortex, respectively.
STN, subthalamic nucleus; GPe, external globus pallidus;
GPi, internal globus pallidus; SNr, substantia nigra pars
reticulta; SNc, substantia nigra pars compacta; VTA,
ventral tegmental area.
NATURE REVIEWS | NEUROSCIENCE
VOLUME 7 | JUNE 2006 | 465
No changes in
Ratio vs interval
05 10 1520
05 10 15 20
Omission and degradation
done using contingency degradation, a procedure that
introduces free rewards that are independent of any
action. Instrumental contingency can be viewed as the
probability of reward given a particular action relative to
the probability of reward given no action. If these prob-
abilities are the same, the contingency is said to be com-
pletely degraded. This would be the case, for example,
if one is paid the same amount regardless of how much
work is done; the question is to what extent work output
would decrease as a result of the degraded contingency
between work and pay. If degrading the contingency
had no effect on work, it could be concluded that the
behaviour was habitual and not goal-directed.
For any given behaviour to be established as a goal-
directed action, it must pass both tests16. First, perform-
ance must be sensitive to revaluation of the outcome.
Second, performance must be sensitive to manipulation
of the A–O contingency. Actions characterized by these
criteria are not defined by specific motor programmes
but by the goal state, such as a certain rate of reward;
in maintaining this goal state the behaviour in question
is modulated bidirectionally. Such bidirectional control
can be demonstrated empirically by a complete reversal
in instrumental contingency known as omission (BOX 1),
in which an action that previously earned a reward is
arranged to prevent it, and the animal can only earn
rewards by refraining from performing the action17,18.
Not surprisingly, omission is the most rapid method for
reducing performance of goal-directed actions.
The analysis of the instrumental actions reviewed
above has crucial implications for the study of habit for-
mation, as behaviour not guided by outcome expectancy
Box 1 | Conditions that lead to habit formation
In ratio schedules, a response results in a certain probability
of reward; more responses yield more rewards. In interval
schedules, a response is only rewarded after a certain time
interval has elapsed. Under certain conditions (for example,
when a single action–outcome (A–O) pairing is used), these
schedules can generate behaviours that differ greatly in
their sensitivity to manipulations of outcome value and
instrumental contingency. For instance, training under an
interval schedule results in behaviour that is less sensitive to
the imposition of the omission contingency17. In short,
whereas ratio schedules produce goal-directed actions
controlled by the A–O contingency, interval schedules tend
to generate stimulus–response (S–R) habits25. The most
crucial difference between these schedules can be
illustrated by plotting their feedback functions, with the
rate of response on the x-axis and the rate of reward on the
y-axis106 (panel a). Whereas ratio schedules set up a strong
correlation between response rates and reward rates,
interval schedules do not13.
Moreover, as Dickinson has observed, in both
overtraining and interval schedules, the experienced
instrumental contingency — the correlation between a
change in response rate and a change in reward rate — is
low24,107. In interval schedules, this experienced
contingency is usually low. However, in ratio schedules the
experienced contingency is high early in training, when
response rates vary, resulting in varying local rates of
reward; but with overtraining, the animals tend to respond
at a consistently high rate, resulting in little change in the
local rates of reward (panel b). Finally, this hypothesis also
explains why, given two actions and two outcomes in
training, behaviour was shown to be goal-directed even
after extensive training with interval schedules14, as this
condition ensures that experienced contingency remains
high (choosing one action would completely stop reward
delivered by the other action).
The feedback function can also be used to illustrate
common manipulations of the instrumental contingency.
For example, omission is a complete reversal of the normal
A–O contingency — that is, a response prevents the
reinforcer, but no response results in reinforcer delivery
(panel c). In degradation, the instrumental contingency is
reduced by presenting non-contingent background
reinforcers; for example, making the probability of the
reinforcer the same regardless of response (panel c).
466 | JUNE 2006 | VOLUME 7
Operationally, the withholding
of reinforcement after previous
and the instrumental contingency can be described as
an S–R habit. This is a clear prediction from S–R/rein-
forcement theory, according to which the outcome is
not part of the S–R association, but merely strengthens
or weakens it. Indeed, under many conditions behav-
iours are not sensitive to changes in contingency and
outcome devaluation19–21. The S–R/reinforcement theory
of Thorndike and Hull has, therefore, stood the test of
time when judged by its success at capturing the nature
of habit learning.
As a result of extensive research, there is now a con-
sensus that instrumental behaviours are controlled by
two distinct systems — the A–O system and the S–R
system — that are engaged under different conditions.
In appetitive instrumental learning, the amount of train-
ing (in particular the number of rewarded responses)
appears to be a crucial factor in determining the shift
from A–O to S–R control over behaviour — that is, habit
formation. Therefore, overtraining tends to promote
habit formation22. The schedule of reinforcement used
is also a key factor (BOX 1). Early studies using devalua-
tion to examine the associative structure of instrumental
conditioning failed to find any evidence that perform-
ance was controlled by goal expectancy, as devaluation
had no effect on performance during the extinction test.
The use of interval schedules in these studies was largely
responsible for their failure to find evidence for A–O
learning19,23,24. An explicit comparison of the schedules
demonstrated that, even with the amount of reinforce-
ment equated, interval schedules produce habitual
responding whereas ratio schedules do not25. The dif-
ference in sensitivity to changes in outcome value must
therefore be due to differences between interval and
ratio schedules (BOX 1).
Habit learning in the dorsal striatum
Early efforts to understand basal ganglia functions
were heavily influenced by S–R/reinforcement theory.
According to the dominant view, the basal ganglia are the
neural implementation of the law of effect, responsible for
S–R learning reinforced by rewards (with the reinforce-
ment signal possibly provided by dopamine) in a gradual
process of habit formation26–28. Unsurprisingly, this view
has initially found considerable empirical support29,30.
Clear evidence comes from studies using the place/
response learning task, first invented by Tolman and
revived by Packard and McGaugh in a series of impor-
tant experiments31,32. In this task, a rat is trained to
retrieve food from one arm of a cross maze surrounded
by various environmental cues (FIG. 2). After training, it
is given probe tests in which the starting arm is placed
at the opposite end of the maze. The use of the response
strategy (same left turn) shows that the learning was
inflexible and response-specific, but the use of the place
strategy (right turn) shows that the animal was able to
incorporate surrounding spatial cues in deciding which
way to turn, selecting a response that was the opposite
of what was initially learned.
After moderate training, most rats used the place strat-
egy when tested, but after extensive training they switched
to a response strategy. Moreover, with inactivation
of the dorsal striatum, the rats were more likely to use
the place strategy despite extended training; however,
inactivation of the hippocampus had the opposite effect
— that is, the response strategy was used more frequently
even early in training32.
These results have two important implications. First,
with overtraining, there is a shift in behavioural control
from goal-directed actions to habits, and such a shift can
be revealed by a behavioural assay. Second, the dorsal
striatum and the hippocampus might, on the basis of
this account, be viewed as competing learning systems.
This view has been developed by Poldrack and Packard,
who argued that direct or indirect neural connections
between the hippocampus and dorsal striatum could
mediate the competition between them33.
Data from human studies suggest that there is a
similar dissociation between declarative learning that
is dependent on the medial temporal lobe (MTL) and
non-declarative striatum-dependent learning. Unlike
habits, declarative memories can be acquired rapidly,
often after a single trial. These memories are explicit, in
that participants are aware of the memories, and they are
flexible, in that they can be applied to new situations. For
example, declarative and habit learning were dissociated
in a recent study using a concurrent discrimination task
in which pairs of objects were presented34. The partici-
pant’s task was to choose the rewarded item in each pair.
Neurologically intact participants learned these dis-
criminations quickly. Patients with severe amnesia fol-
lowing damage to the MTL were also able to learn these
discriminations, but their performance improved much
more slowly. Although the patients eventually learned
the discriminations, they did not show explicit knowl-
edge of these associations. They were unable to choose
the rewarded items from the total array of stimuli. Their
performance appeared to be habitual, with the presenta-
tion of the pair automatically eliciting the choice of the
correct item. Indeed, the amnesic participants justified
their choices by stating that some items “just seemed
right”, rather than relying on their declarative memory
for previous trials.
Another task that has been used to assess habit learn-
ing in humans is the probabilistic classification task. In
this task, a series of cues are each probabilistically asso-
ciated with one of two outcomes, and the participant
must guess which outcome is predicted on the basis
of the cues that appear in each trial. Because the cues
and outcomes are probabilistically associated, it is dif-
ficult to memorize their relationship explicitly. Amnesic
patients are able to learn these associations normally,
which is consistent with the idea that they are learned
independently of MTL structures that support declara-
tive memory. Furthermore, patients with Parkinson’s
disease, who exhibit abnormal striatal functioning due
to loss of dopaminergic input, have been shown to be
impaired in the implicit learning of these associations35,
although they managed to achieve normal levels of per-
formance with further training. This suggests that other
neural systems can support learning in this task. A recent
study found that patients with mild Parkinson’s disease
were able to perform almost as well as neurologically
NATURE REVIEWS | NEUROSCIENCE
VOLUME 7 | JUNE 2006 | 467
Win-stay on a radial arm maze
normal participants on the probabilistic classification
task, but they showed a very different pattern of brain
activation during performance as revealed by functional
MRI. Whereas in control participants the striatal regions
were activated during learning, patients with Parkinson’s
disease showed activation in the hippocampus and sur-
rounding MTL cortical regions36. It appears that patients
with Parkinson’s disease achieved good performance by
relying on declarative memory, whereas neurologically
intact participants relied on non-declarative learning
mechanisms. Many real-world tasks encountered by
humans probably involve both habit and declarative
learning; the system that contributes most to perform-
ance depends on the amount of training, the ease of
memorizing associations and the relative integrity of
the basal ganglia and MTL in the learner.
Functional heterogeneity in the dorsal striatum. Despite
the evidence for basal ganglia involvement in habit
learning, many findings cannot be explained by the idea
that the dorsal striatum is the substrate of this type of
learning. For example, studies recording from caudate
cells in monkeys performing a saccade task have shown
that the neural activity encoding the preferred direction
of saccade could change according to whether that direc-
tion is rewarded, and this activity is rapidly modified as
new contingencies are encountered37–39. Simultaneous
recording from the prefrontal cortex (PFC) and caudate
has shown that caudate activity rapidly adapts to the
contingency before PFC activity does, and even before
significant improvements in performance occur40. Such
data suggest that certain learning mechanisms in the
striatum do not have the characteristics of habit learn-
ing, that anticipation of future rewards has a crucial role
in regulating striatal activity, and that changes in neural
activity as a result of learning occur at a rate too rapid to
be explained by the slow and gradual changes posited by
traditional S–R/reinforcement theory.
Because the dorsal striatum is a large and het-
erogeneous structure, similar to the cerebral cortex,
the question naturally arises as to whether, like the
cortex, it is also functionally specialized. The caudate
in primates is part of the ‘associative striatum’, which
receives inputs from association cortices. It corre-
sponds to the dorsomedial striatum (DMS) in rodents,
whereas the putamen is part of the sensorimotor
striatum, corresponding to the dorsolateral striatum
(DLS) in rodents41 (FIG. 3a). Many investigators have
created large lesions of the dorsal striatum in rodents,
without regard for the medial/lateral distinction, but
the damage appears to have been more prominent in
the lateral region.
Indeed, the DLS differs from the DMS in connectiv-
ity, distribution of various receptors and mechanisms of
synaptic plasticity41–43 (BOX 2). Previous studies have also
suggested a functional dissociation between the DLS
and DMS42,44. For example, work by Devan and White
showed that the DMS, like the dorsal hippocampus, is
involved in flexible place learning, whereas the DLS sub-
serves inflexible response learning45,46. In particular, they
discovered that lesions of the DMS result in a preference
for cue-based responding in the water-maze task. Taking
into account these results and the different patterns of
anatomical connectivity, these investigators proposed
that the DMS belongs to the same functional system as
In view of the distinction between actions and
habits outlined above, these considerations raise the
interesting possibility that the DLS is involved in
S–R learning, whereas the DMS is involved in A–O
learning. Yin et al. conducted a series of studies to
test this hypothesis using assays (BOX 1) that could be
Figure 2 | Simple maze tasks for measuring habits and actions. a | In the place/response task, rats are trained to
retrieve food from one arm of a T-maze or cross maze. The content of learning can be assessed by moving the starting arm
to the other side of the maze on a probe test. The animal may enter the arm corresponding to the location of the reward
during training (place strategy) or the arm corresponding to the turning response that was reinforced during training
(response strategy). b | In the radial arm maze, animals can learn either a win-stay or a win-shift contingency. In win-stay,
arms baited with food are signalled by a cue (such as a light at the entryway). Animals will gradually learn to respond to
these cues by running down the arms and retrieving the food. Extensive win-stay training produces behaviour insensitive
to devaluation113, and requires the dorsolateral striatum114. By contrast, the win-shift task is similar to natural foraging in
that animals need to efficiently traverse the region without revisiting areas before resources are replenished. They must
learn the location of the arms that they have visited on each trial. Because arms are not re-baited on each trial, once the
animal visits the arm and eats the food, it should remember not to return to that arm during the session. Win-shift
performance is sensitive to devaluation113, and is impaired by hippocampal lesions114.
468 | JUNE 2006 | VOLUME 7
Increasing effector specificity and automaticity
DA neuronsDA neurons DA neurons
DA neurons DA neurons
applied to instrumental learning paradigms17,21,47–49.
Taking advantage of the established differences
between ratio and interval feedback schedules, they
first examined the effects of excitotoxic lesions to
the DLS using variable interval schedules, which are
known to generate habits — in this case, lever press-
ing that is insensitive to outcome devaluation. After
training, the sucrose reward was devalued by inducing
taste aversion until the animals stopped consuming
it in their home cages. When these rats were tested
later for extinction, lever pressing of controls was not
reduced by devaluation. By contrast, although rats
with DLS lesions could normally learn to press a lever
for reward, they made fewer responses after devalu-
ation relative to the controls. It appears that because
their habit system was disrupted by the lesion, the
alternative A–O system assumed control over behav-
iour. However, a similar effect was not observed in rats
with DMS lesions.
In another study, to assess the role of the DMS in A–O
learning, Yin et al. used a training procedure with two
actions and two outcomes under variable ratio sched-
ules. This procedure generates goal-directed actions that
are sensitive to outcome devaluation and contingency
degradation14. The posterior DMS (pDMS) was shown to
be a crucial substrate for the acquisition and expression
of goal-directed actions. Both pre- and post-training
lesions, as well as reversible inactivation of the pDMS
Figure 3 | Cortico-basal ganglia networks as the fundamental motifs of cerebral organization. a | Highly simplified
schematic illustration of the three major networks: the limbic, associative and sensorimotor networks. b | Schematic
illustration showing cortico-basal ganglia networks in relation to serial adaptation. A shift from the associative to the
sensorimotor cortico-basal ganglia network is observed during habit formation. DA, dopamine; DLS, dorsolateral striatum;
DMS, dorsomedial striatum; PFC, prefrontal cortex.
NATURE REVIEWS | NEUROSCIENCE
VOLUME 7 | JUNE 2006 | 469
abolished sensitivity to devaluation and degradation48.
Moreover, local blockade of NMDA (N-methyl-d-aspar-
tate) receptors, which are required for the induction of
long-term potentiation (LTP) in this region, specifically
prevented the encoding of new A–O contingencies
without impairing performance47. Therefore, the pDMS
appears to be a crucial neural substrate for the learning
and expression of goal-directed actions. In its absence,
the behaviour of the animal becomes habitual even
under training conditions that result in goal-directed
actions in control rats.
Moreover, it was shown that the pDMS is also involved
in flexible choice behaviour in the place/response task on
a cross maze49. After pre-training lesions were created,
rats were trained extensively to retrieve food from the
east arm of the maze, starting from the south arm, by
turning right at the choice point (FIG. 2). Unlike control
rats, most rats in the pDMS lesion group turned right
on the probe tests, when they started from the north
arm. This observation agrees with a growing body of
recent data that show the role of the DMS in flexible
choice behaviour50,51. Note that the key manipulation
in the place/response task, namely the probe test with
the opposite starting point, is similar to a reversal in the
A–O contingency. Previously, a particular turn would
lead to the arm with food, but with the 180˚ rotation
of the starting point, the same turn would lead to the
previously unrewarded arm. Again, the choice behav-
iour of rats with pDMS lesions is rendered inflexible and
Lever-pressing controlled by the instrumental con-
tingency therefore shares common neural substrates
with the use of the place strategy in the maze. Despite
differences between the motor programmes of pressing
a lever and of traversing a maze, the common neural
substrate in the pDMS suggests that this area is crucial
for learning the A–O contingency, the feature shared by
these tasks. On the cross maze, after a reversal in starting
point, reaching the original goal requires a reintegration
of the spatial features of the environment with the goal
location. Whereas the hippocampus is necessary to
ascertain the spatial location of the reward, the pDMS
is involved in choosing the correct course of action that
leads to this location.
One interpretation of these results is that the hippoc-
ampus does not compete with, or function independ-
ently of, the striatum, as has been previously claimed29,33.
Rather, the hippocampus can act together with dorso-
medial and ventral striatal regions to form a functional
circuit. This hypothesis is supported by studies that
examined activity in the DMS during spatial navigation
on various mazes52,53. According to these studies, the
DMS contains spatially selective neurons that fire when
animals take a particular route to reach a goal; it also
contains head-direction neurons with activity aligned
with that of the place fields of hippocampal place cells.
Therefore, information about the current position of the
animal provided by hippocampal place cells can be used
to signal where to go to reach a definite goal, and this
information is probably conveyed to the DMS directly
via the cortico-striatal projection from the hippocampal
Further evidence for the role of the associative stria-
tum in A–O learning has come from studies examining
caudate (DMS homologue) activity in humans and
other primates54–56. Tricomi et al.57 found that caudate
activity was modulated by the perceived contingency
between action and outcome. Robust activation was
found only when the participants thought that their
action resulted in the gain or loss of money, whereas
Box 2 | Different rules of synaptic plasticity
A basic assumption in contemporary neuroscience is that long-term synaptic plasticity, widely studied in the forms of long-
term potentiation (LTP) and long-term depression (LTD), is a central physiological mechanism that underlies learning. The
dissociation between the dorsolateral striatum (DLS) and dorsomedial striatum (DMS) at the level of behaviour is mirrored
by distinct rules of synaptic plasticity in these regions. Although dopamine is crucial for all forms of striatal plasticity, the
exact mechanisms show remarkable regional variation43.
The DMS expresses LTP that depends on the activation of D1-like dopamine receptors and NMDA (N-methyl-d-aspartate)
glutamate receptors43,108. The blockade of NMDA receptors in this region specifically prevents the learning of action–
outcome contingency, suggesting a critical functional role for LTP in the DMS in such learning47. Additional evidence
comes from a study using intracranial self-stimulation of the dopaminergic cells in rats to reinforce lever pressing109. The
optimal parameters for self-stimulation were also found to induce cortico-striatal LTP in vivo, and the degree of
potentiation in the cortico-striatal pathway in the DMS negatively correlated with the time taken to acquire lever pressing,
which is a measure of initial action–outcome learning. This form of LTP requires the activation of D1 receptors, suggesting
that it is the same form as is observed in vitro.
By contrast, dopamine-dependent striatal LTD is usually found in the DLS, and requires the activation of D2-like
dopamine receptors, group I metabotropic glutamate receptors, and L-type calcium channels110. The resulting increase in
intracellular calcium causes the postsynaptic synthesis and the release of endocannabinoids, which then act as a
retrograde messenger on presynaptic cannabinoid CB1 receptors to decrease probability of glutamate release from the
cortico-striatal terminals111. The role of this intriguing form of plasticity in DLS-dependent habit learning is not known.
However, previous work has shown that local infusion of a D2 receptor agonist can improve acquisition on the win-stay
task, which typically produces habitual responding that is insensitive to outcome devaluation112,113.
As the above observations suggest, the same learning experience can result in different types of synaptic change in the
DLS and DMS. These changes are regulated by distinct rules as a result of differential distribution of key receptors in these
regions. Future studies will no doubt shed light on this striking correlation between mechanisms of striatal plasticity at the
cellular and molecular level and the action/habit dissociation at the behavioural level.
470 | JUNE 2006 | VOLUME 7
time-locked anticipation of the outcome without the action
contingency did not activate the caudate. These results
also clearly implicate the associative striatum as a crucial
component of the A–O system. Furthermore, Williams
and Eskandar recorded neural activity from both the
anterior caudate and the putamen (DLS homologue) in
monkeys trained to move joysticks after presentations
of discriminative stimuli58. These authors showed that
caudate activity in response to outcome presentation
is strongly correlated with the rate of learning (slope
of the learning curve), whereas putamen activity is
correlated with the learning curve itself. Although the
authors interpreted such learning as S–R, in view of
the framework above, the behaviour of the monkeys
is probably controlled by the A–O contingency. The
specific discriminative stimuli merely tells the animal
which A–O contingency is in effect (that is, that a par-
ticular joystick movement will lead to reward), and the
learning that occurs during the steepest portion of the
learning curve corresponds to the initial acquisition of
the A–O association. However, once this rapid learn-
ing has taken place, caudate activity quickly decreases,
whereas putamen activity remains high and follows the
learning curve closely until it asymptotes. This pattern
of activity agrees with earlier theoretical claims about
the relative rates of learning in the A–O and S–R sys-
tems59. Moreover, this study also found that, whereas
stimulation of the putamen had no effect, stimulation of
the caudate significantly enhanced the rate of learning
without changing the asymptotic level of performance
or hedonic preference, suggesting a causal role for this
structure in instrumental learning.
A hierarchy of cortico-basal ganglia networks
We have suggested that associative structures — abstract
descriptions of learning processes at the behavioural level
— can be mapped onto discrete regions in the dorsal
striatum. In particular, A–O learning can be mapped
onto the DMS, whereas S–R learning can be mapped onto
the DLS. How, then, are we to interpret such demonstra-
tions of functional heterogeneity from studies that use the
strategy of process dissociation? More importantly, what
does it tell us about habit formation, whereby behavioural
control is switched from one system to another?
Paradoxically, the chief implication of such func-
tional heterogeneity is not that a more refined analysis
of behaviour is accompanied by a more refined localiza-
tion of function. If we compare the relevant data on the
striatum with data from other brain regions that project
to, or receive inputs from, the basal ganglia, a different
Considerable evidence shows that the PFC also
has a crucial role in instrumental learning60–65. Studies
by Balleine and colleagues have shown that rats with
pre-training lesions to the medial PFC, especially the
prelimbic region, which provides massive projections
to the DMS, failed to show sensitivity to devaluation
and degradation60,61. In addition, pre-training lesions of
the mediodorsal nucleus of the thalamus, an eventual
downstream target of outputs from the DMS as well as
the major source of thalamic projections to the PFC, also
abolish sensitivity to devaluation and degradation66. To
a certain extent, these observations resemble the effects
of the pDMS lesions reviewed above67.
Taking into account the above observations, we can
no longer maintain that the dorsal striatum as a whole is
a substrate for habit learning. Nor can we capture the dis-
tinction adequately with the traditional contrast between
hippocampus-dependent learning and striatum-depend-
ent learning. It should be noted that in this connection,
selective pre-training lesions of the hippocampus do not
consistently render behaviour habitual, as lesions of the
pDMS do68. One possible role for the hippocampus, in
view of this result and of the results from previous maze
studies31,46,69, is the integration of goal-directed actions
that require some representation of spatial and/or tem-
poral configurations. In any case, although the precise
role of the hippocampus in A–O learning remains to be
determined, the considerable functional heterogeneity
in the dorsal striatum prompts a reconsideration of
the currently accepted model of multiple memory sys-
tems in which the striatum as a whole serves a specific
Alternatively, we propose that a cortico-basal ganglia
network is a fundamental motif of cerebral organization,
and is the fundamental unit of function at the level of
behaviour (FIG. 3a). This claim is inspired by the tradi-
tional model of basal ganglia organization in terms of
parallel and re-entrant loops70, although we do not place
special emphasis on either the thalamocortical target of
basal ganglia outputs or the strictly parallel nature of
the networks. Indeed, as discussed below, interaction
between networks is vital to the transformation from
actions to habits.
A cortico-basal ganglia network is a functional
group comprising different cortical, striatal and pallidal
components, in addition to the various cell groups (for
example, dopaminergic) in the midbrain that constitute
the brain’s value system, as well as the associated dien-
cephalic structures (for example, the thalamus and the
subthalamic nucleus). The integration of various physi-
ological processes in these components results in the
output of the network — that is, behaviour. Although
each of these components, by virtue of characteristic
physiological properties, has unique ‘computational’
properties, at the behavioural level it is the integrated
functioning of a distributed network comprising vari-
ous components that is important. That is, when we
probe behaviour with contemporary behavioural assays,
we can map dissociable classes of behaviours onto dis-
sociable cortico-basal ganglia networks. This point is
worth emphasizing, as systems neuroscience is often
dominated by attempts to localize psychological func-
tions without regard for the actual functional circuitry
of the brain. Not only do the psychological functions
lack operational specificity, but the anatomical entities
that are said to subserve such functions also lack the
requisite circuitry. For instance, it is often asserted that
the neocortex mediates a particular function, whereas
the striatum subserves another40. By contrast, using
operationally defined representational structures that
can be dissociated behaviourally allows us to identify
NATURE REVIEWS | NEUROSCIENCE
VOLUME 7 | JUNE 2006 | 471
the distributed networks that control distinct types of
decision-making and learning. Although our proposal
remains preliminary, and needs to be refined and cor-
rected by future research, it should be clear by now
that the traditional view of multiple memory systems
(which divides the cerebrum into distinct functional
systems corresponding to visually distinct anatomical
entities such as the hippocampus, amygdala, striatum
and neocortex) does not provide a fully satisfactory
In the framework proposed here, the corticostriatal
projections are loosely organized by cortical region so
that the limbic cortex projects to the limbic striatum
(mainly the nucleus accumbens), the association cortex
projects to the dorsomedial, or associative, striatum, and
the sensorimotor cortex projects to the dorsolateral or
sensorimotor striatum71 (FIG. 3a). The limbic network,
which has a key role in appetitive Pavlovian learning,
can exert tremendous influence on the associative and
sensorimotor networks (discussed below).
In the associative network, the medial PFC (similar
to the dorsolateral PFC in primates72) and the DMS
(caudate) are involved in transient or ‘working’ memory.
Lesions of either structure impair performance on spatial
delayed response and delayed alternation tasks7,73,74. Like
the PFC62, caudate activity is also strongly modulated by
anticipation of reward75. Thus, the associative network is
capable of monitoring recent actions as well as anticipat-
ing their consequences. By contrast, the sensorimotor
level comprises the sensorimotor cortices and their tar-
gets in the basal ganglia, beginning with the DLS. The
outputs of this circuit eventually reach the motor cortices
and brainstem motor networks. Unlike the associative
striatum, neural activity in the sensorimotor striatum
is not directly modulated by reward expectancy, but is
more closely related to movements and to discriminative
Habit formation and serial adaptation. Joel and Weiner
proposed an important revision to the traditional scheme
of parallel circuits41,78,79. Rather than closed loops with
strict point-to-point topographical organization, they
argued that interaction between different loops is made
possible by interconnections between them. This claim
is supported by recent anatomical work. In addition to
the closed, strictly reciprocal projections, there are open
striatonigral projections to a nigral area that, in turn,
projects to a different striatal region80. These connec-
tions could allow the activity in one cortico-basal ganglia
circuit to be propagated to the next circuit iteratively,
suggesting a hierarchical organization in which a given
cortico-basal ganglia circuit can be considered as a par-
ticular level in a functional hierarchy81. In addition, fur-
ther interaction between circuits is possible at the level
of the thalamo-cortico-thalamic connections82.
We therefore propose that these overlapping
cortico-basal ganglia networks form a labile hierarchy
with three major levels, consisting of the limbic (stimu-
lus–outcome, S–O), associative (A–O) and sensorimotor
(S–R) networks (FIG. 3a). Here, we focus on the last two
networks (FIG. 3b), which we locate in the two cortico-basal
ganglia circuits coursing through the dorsal striatum.
These networks are characterized by strong re-entrant
projections to the thalamocortical network, often pre-
cisely re-entering the cortical region from which the
corticostriatal projections arise83. The associative net-
work is crucial for the acquisition and performance
of goal-directed actions, but in the course of habit
formation this network appears to relinquish control
over behaviour to the sensorimotor network, which is
responsible for S–R habits. This relationship is most
clearly revealed in two related sets of observations: one
on differences in the extent of effector specificity, and the
other on the switch, with extended practise, from one
network to another in the control of behaviour.
Effector specificity refers to the extent to which the
learning of a skill, as reflected in various performance
measures, is limited to the effector (for example, a hand)
with which it is originally trained. As shown by a study
using monkeys, correct performance early in the learn-
ing of a behavioural sequence is not specific to the hand
originally used to perform the sequence; with extensive
practise, however, correct performance becomes spe-
cific to the hand used84. This task, not surprisingly, also
requires the striatum, and learning of new and older
sequences depends on different striatal regions.
The degree of effector specificity reflects the level of
functional integration in the hierarchical organization of
cortico-basal ganglia networks. The associative network
achieves a higher level of functional integration, having at
its disposal a wider range of motor programmes that can
be selected to reach the goal. It is not effector-specific,
possibly owing to the bilateral corticostriatal projections
in this network. By contrast, the sensorimotor network
is more effector-specific, possibly owing to its more
lateralized corticostriatal projections85. With habit for-
mation, therefore, the control of behaviour shifts from
a higher level of functional integration to a lower one
— more specifically, from the associative cortico-basal
ganglia network to the sensorimotor cortico-basal gan-
glia network (FIG. 3b). However, extensive damage to
either network results in the other network assuming
control over instrumental behaviour17,21,47–49,60.
Human imaging studies of habit learning have
found that overtraining of a behaviour shifts the cor-
tical substrate from ventral areas to more dorsal areas,
and similar shifts have been observed in the striatum.
Learning of new motor responses, for example, acti-
vated the caudate and the dorsolateral PFC, whereas
with well-learned sequences the site of activation shifts
to the putamen and motor cortices. When well-trained
participants were asked to pay attention to their actions,
the caudate and the more ventral PFC were again acti-
vated86,87. Such findings are not surprising in light of the
hierarchical framework. Therefore, attention to action
requires the associative network, but once a task is well
learned only the sensorimotor network is needed for its
In another study, Poldrack et al. examined the neural
basis of automaticity, a concept from cognitive psychol-
ogy operationally defined as resistance to interference
from the performance of a secondary task88. After
472 | JUNE 2006 | VOLUME 7
∆ response rate
∆ outcome rate
A reinforcement learning
method that is driven by the
difference between temporally
successive predictions, rather
than by the difference between
predicted and actual
Markov decision processes
A stochastic control process
with the Markov property:
future states are conditionally
independent of past states and
depend only on the current
extensive training, the associative cortico-basal ganglia
network, including the dorsolateral PFC and its cor-
responding striatal target in the caudate, decreased in
activity. However, the supplementary motor area and
the putamen/globus pallidus, parts of the sensorimotor
cortico-basal ganglia network, did not show a similar
decrease. As behaviour became more automatic with
extensive practise, there was also a shift from the associa-
tive to the sensorimotor cortico-basal ganglia networks.
Potential mechanisms for serial adaptation. What are
the mechanisms underlying the processes of serial
adaptation described above? Unfortunately, there is
little evidence available to answer this question. As
mentioned above, the spiralling connections between
the striatum and the midbrain discovered by Haber and
colleagues could serve as a possible anatomical instan-
tiation of links between networks, but numerous other
possibilities exist82. Without indulging in speculative
anatomy, we discuss the problem at a more abstract,
computational level, which is open to different neural
As described in BOX 1, Dickinson first proposed that
the experienced contingency between behaviour and
reward is the key determinant of whether behaviour is
goal-directed or habitual. Experienced contingency is
defined as the correlation between changes in reward
rates and changes in response rates. This account has
implications for possible neural implementations. It sug-
gests that there are neural detectors for rates of responses
and rates of outcomes, and that outputs from these
detectors must converge to yield some estimate of ‘expe-
rienced contingency’, which could determine whether
the A–O system or the S–R system is engaged. To detect
rates and changes in rates, a process akin to differentia-
tion would be appropriate. For example, as illustrated by
FIG. 4, activity in a particular unit could simply reflect the
derivative (for example, rate) of activity upstream, and
an iteration of this process could readily yield the second
derivative (for example, a change in rate). Although our
framework implicates the cortico-basal ganglia networks
as the neural implementations of such computational
processes, identifying the specific substrates requires
extensive empirical work. This simple mechanism sug-
gests that any reduction in experienced instrumental
contingency, as encountered in contingency degradation
and overtraining, could lead to reduced output of the
contingency detector, and it is this output that would
compete with the S–R/reinforcement system for the
control of behaviour.
A different and more formal model, which accounts
for much of the data on the various conditions leading
to habit formation, was provided by a recent theoretical
paper89. Using a set of computational methods known as
reinforcement learning, Daw et al. modelled the process
of habit formation by combining two independent con-
trollers with distinct mechanisms for estimating value
functions (the ‘yield’ of behaviour in a given state). The
‘model-based’ controller was used to simulate the A–O
system, whereas the ‘model-free’ controller was used to
simulate the S–R habit system. The key proposal was that
arbitration is based on the uncertainty (posterior vari-
ances of estimated values or expected inaccuracy) in esti-
mating the value function; the value determining actual
choice behaviour is taken from the controller with the
least uncertainty. According to Daw et al., the model-free
(habit) controller, using the temporal-difference algorithm,
estimates value functions by caching — that is, storing a
long-run value for future use — and choice behaviour is
determined by the stored value. Because such estimates
are divorced from the outcome (much like the S–R rein-
forcement theory), this method is computationally trac-
table but inflexible, yielding behaviour that is insensitive
to outcome devaluation, whereas exactly the opposite
is true of the model-based controller (A–O system).
Further work is needed to extend the uncertainty-based
model beyond discrete Markov decision processes to truly
free operant conditions, and to incorporate instrumental
contingency into this model.
Habits in relation to addiction
Addiction has often been viewed simply as a maladaptive
type of habit learning90. Although this view is supported
by the insensitivity of drug-seeking behaviour to harm-
ful consequences, the motivational compulsion seen in
addiction can hardly be explained by S–R/reinforcement
theory alone. Although our suggestion that habit for-
mation involves the serial adaptation of distinct cortico-
basal ganglia networks is also supported by the literature
on addiction91,92, in the case of addiction considerations
must be given to additional processes, especially appe-
titive Pavlovian conditioning, as incidental pairing
between situational cues and drugs allow such learning
Figure 4 | Schematic illustration of hypothetical mechanisms for the detection of
instrumental contingency in appetitive instrumental learning. The most
straightforward mechanism for the detection of rates and changes in rates is the
biological equivalent of differentiation. Anticipation is made possible by a higher-
order derivative of the detected variable, just as velocity can increase more quickly
than distance. Therefore, in the neural implementation of differentiation we already
have a possible mechanism for prediction. The output of the ‘experienced contingency
detector’ should have a crucial role in determining whether the action–outcome (A–O)
system or the stimulus–response (S–R) system is controlling behaviour. In the absence
of any activation of this detector, the S–R system, as described by traditional S–R/
reinforcement theory, can assume control over behaviour. In this illustration we have
also assumed that the contiguity between response and outcome reinforces the S–R
NATURE REVIEWS | NEUROSCIENCE
VOLUME 7 | JUNE 2006 | 473
Repetitive patterns of
behaviour that are
characterized by the lack of
variation; often observed in
various psychiatric disorders
and after psychomotor
A patch-like compartment in
the striatum that is
characterized by low acetyl-
cholinesterase staining and
other chemical markers.
to take place. In most situations, of course, Pavlovian
conditioning and instrumental learning can occur
simultaneously, and interact in controlling behaviour.
In our view, to understand addiction it is necessary to
consider these interactions.
In Pavlovian conditioning, the contingent pairing
of a conditional stimulus (CS) and an outcome results
in the acquisition of conditional responses (CRs) to the
previously neutral stimulus. The CR is not controlled by
the response–outcome contingency: even if the response
prevents the outcome, as when an omission contingency
(BOX 1) is imposed, the CR is still elicited by the CS93.
As Berridge and Robinson have argued, situational
cues in addiction can acquire motivational properties,
which they call ‘incentive salience’94. Incentive salience is
a measure of how much the reward is ‘wanted’ rather than
‘liked’, and it is this property that is argued to be greatly
enhanced in addiction. Being a description of appetitive
preparatory CRs, it can be dissociated from consum-
matory CRs such as taste reactivity8,95. Preparatory CRs
are usually less specific than consummatory CRs (for
example, salivation); although measurable peripherally,
they also correspond to central motivational states such as
craving or wanting in appetitive learning, or fear in aver-
sive learning8. Such states induced by predictors of reward
can directly potentiate instrumental responding8,96.
It has long been claimed that discriminative stimuli
preceding instrumental actions and reafferent stimuli
generated by actions can form associations with the
outcome and further motivate instrumental behaviour97.
Although such explanations fail to account for much of
the contemporary data, they remain valuable for their
emphasis on Pavlovian–instrumental interactions, which
have been amply documented24. Pavlovian–instrumental
transfer (PIT), a rigorous experimental method used to
study such interactions, assesses the extent to which
Pavlovian CSs that predict outcomes can potentiate
instrumental performance yielding the same outcomes98.
As PIT is normally produced by long, tonic CSs, which
can also elicit preparatory CRs in appetitive conditioning,
one potentially important mechanism underlying addic-
tion at the level of neural systems is the heightened trans-
fer from the Pavlovian incentive system to the systems
that govern instrumental behaviour8. This mechanism is
in accord with the important role of environmental cues
in triggering compulsive drug seeking91.
In view of the serial adaptation hypothesis described
above, PIT can also be viewed in terms of interactions
between cortico-basal ganglia networks (FIG. 3a). In
this connection, an intriguing recent finding is that
as behaviour becomes habitual it also becomes more
susceptible to transfer of control — that is, a Pavlovian
CS can potentiate habitual responding more than it
can potentiate goal-directed actions99. As the nucleus
accumbens, which belongs to the limbic cortico-basal
ganglia network, is critical for PIT100, it could also exert
control over the sensorimotor network (FIG. 3a) via the
spiralling connections with dopaminergic neurons80.
Similar ideas have been advanced recently by
Canales, whose argument is based on experiments that
measure activity in different chemical compartments in
the striatum5. Work by Canales and Graybiel has shown
that exposure to addictive drugs leads to relatively higher
activation of striosomal neurons than of matrix neurons,
and that this pattern of activation is correlated with a
measure of motor stereotypy101. These two compartments
generally delineate two sources of cortical inputs to the
striatum, and so Canales argues that the dominance of
the striosomal activation reflects heightened control of
the basal ganglia circuitry by inputs from limbic cortical
areas. This hypothesis is supported by the finding that
lesioning or inactivating the infralimbic cortex, which
is involved in the inhibitory control of Pavlovian CRs102
and a source of inputs to the striosome compartment,
resulted in sensitivity to devaluation even in overtrained
rats whose performance is normally habitually control-
led103,104. Although the role of the infralimbic–striosome
system in habit formation is not clear, it may in fact be
engaged in Pavlovian control of instrumental systems.
An obvious prediction here is that lesions of this system
would disrupt PIT.
What is clear from the above discussion is that the
motivational compulsion seen in addiction could be
modelled by PIT, and implemented by links between the
limbic and the sensorimotor cortico-basal ganglia net-
works (FIG. 3a). Accordingly, different stages of addiction
are expected to be characterized by distinct behavioural
characteristics as a result of the underlying serial adapta-
tion from network to network. In support of such claims,
a recent study of the effect of cocaine self-administration
on striatal activity in monkeys found a gradual spread
and intensification of the effects of the drug from the
ventral striatum to the dorsal striatum92. Everitt and
Robbins have also shown that reafferent stimuli that
predict reward can initially potentiate dopamine release
in the accumbens, and eventually in the dorsal striatum,
which suggests that these Pavlovian motivators can affect
cortico-basal ganglia networks that mediate instrumen-
tal behaviour105. Pavlovian learning, therefore, possibly
precedes instrumental learning, with serial adaptation
initiated in the limbic network and eventually spreading
to the sensorimotor network. As a result, our general
framework can readily incorporate various accounts of
addiction, and establish a relationship between habitual
responding and motivational compulsion.
Given the enormous structural complexity of the basal
ganglia, a strictly bottom-up approach in elucidating
their functions might not be fruitful. Instead, research
can be guided by a top-down analysis based on the
understanding of behaviour. The goal of this review,
above all, is to clear up conceptual confusions and stimu-
late research by outlining a coherent framework based
on known anatomy and physiology as well as our current
understanding of instrumental behaviours.
Central to this framework is the distinction between
goal-directed actions and stimulus-driven habits, the
two main categories of instrumental behaviour. They
can be dissociated at the behavioural level using assays
that manipulate the value of the outcome and the contin-
gency between action and outcome. Using these assays,
474 | JUNE 2006 | VOLUME 7
Swanson, L. W. Cerebral hemisphere regulation of
motivated behavior. Brain Res. 886, 113–164 (2000).
A learned and provocative review of cerebral
anatomy focusing on basal ganglia organization.
Wilson, C. J. in The Synaptic Organization of the Brain
(ed. Shepherd, G. M.) 329–375 (Oxford Univ. Press,
New York, 2004).
Deniau, J. M. & Chevalier, G. Disinhibition as a basic
process in the expression of striatal functions. II. The
striato-nigral influence on thalamocortical cells of the
ventromedial thalamic nucleus. Brain Res. 334,
Albin, R. L., Young, A. B. & Penney, J. B. The functional
anatomy of basal ganglia disorders. Trends Neurosci.
12, 366–375 (1989).
Canales, J. J. Stimulant-induced adaptations in
neostriatal matrix and striosome systems: transiting
from instrumental responding to habitual behavior in
drug addiction. Neurobiol. Learn. Mem. 83, 93–103
Wickens, J. R. & Koetter, R. in Models of Information
Processing in the Basal Ganglia (eds Houk, J. C.,
Davis, J. L. & Beiser, D. G.)187–214 (MIT Press,
Cambridge, Massachusetts, 1995).
Divac, I., Rosvold, H. E. & Szwarcbart, M. K. Behavioral
effects of selective ablation of the caudate nucleus.
J. Comp. Physiol. Psychol. 63, 184–190 (1967).
Konorski, J. Integrative Activity of the Brain (University
of Chicago Press, Chicago, 1967).
Skinner, B. The Behavior of Organisms (Appleton-
Century-Crofts, New York, 1938).
10. Tolman, E. C. Purposive Behavior in Animals and Man
(Macmillan, New York, 1932).
11. Thorndike, E. L. Animal Intelligence: Experimental
Studies (Macmillan, New York, 1911).
12. Hull, C. Principles of Behavior (Appleton-Century-
Crofts, New York, 1943).
13. Dickinson, A. in Animal Learning and Cognition
(ed. Mackintosh, N. J.) 45–79 (Academic, Orlando,
14. Colwill, R. M. & Rescorla, R. A. in The Psychology of
Learning and Motivation (ed. Bower, G.) 55–104
(Academic, New York, 1986).
References 13 and 14 are excellent introductions
to the modern study of instrumental learning.
15. Hammond, L. J. The effect of contingency upon the
appetitive conditioning of free-operant behavior.
J. Exp. Anal. Behav. 34, 297–304 (1980).
16. Dickinson, A. & Balleine, B. in Spatial Representation:
Problems in Philosophy and Psychology (eds Eilan, N.
et al.) 277–293 (Blackwell, Malden, Massachusetts,
17. Yin, H. H., Knowlton, B. J. & Balleine, B. W. Inactivation
of dorsolateral striatum enhances sensitivity to changes
in the action–outcome contingency in instrumental
conditioning. Behav. Brain Res. 166, 189–196 (2006).
18. Davis, J. & Bitterman, M. E. Differential reinforcement
of other behavior (DRO): a yoked-control comparison.
J. Exp. Anal. Behav. 15, 237–241 (1971).
19. Holman, E. W. Some conditions for the dissociation of
consummatory and instrumental behavior in rats.
Learn. Motiv. 6, 358–366 (1975).
20. Adams, C. D. Variations in the sensitivity of
instrumental responding to reinforcer devaluation.
Q. J. Exp. Psychol. 33B, 109–122 (1982).
21. Yin, H. H., Knowlton, B. J. & Balleine, B. W. Lesions of
dorsolateral striatum preserve outcome expectancy
but disrupt habit formation in instrumental learning.
Eur. J. Neurosci. 19, 181–189 (2004).
22. Colwill, R., Rescorla, R. A. The role of response–
reinforcer associations increases throughout extended
instrumental training. Anim. Learn. Behav. 16,
23. Dickinson, A. in Learning, Motivation, and Cognition
(eds Bouton, M. E. & Fanselow, M. S.) 345–367
(American Psychological Association, Washington DC,
24. Dickinson, A. in Contemporary Learning Theories
(eds Klein, S. B. & Mowrer, R. R.) 279–308 (Lawrence
Erlbaum Associates, Hillsdale, New Jersey, 1989).
25. Dickinson, A., Nicholas, D. J. & Adams, C. D. The
effect of the instrumental training contingency on
susceptibility to reinforcer devaluation. Q. J. Exp.
Psychol. B 35, 35–51 (1983).
26. Miller, R. Meaning and Purpose in the Intact Brain
(Oxford Univ. Press, New York, 1981).
27. Mishkin, M., Malamut, B. & Bachevalier, J.
in Neurobiology of Learning and Memory
(eds Lynch, G. et al.) 65–77 (Guilford, New York, 1984).
28. Robbins, T. W., Giardini, V., Jones, G. H., Reading, P. &
Sahakian, B. J. Effects of dopamine depletion from the
caudate-putamen and nucleus accumbens septi on the
acquisition and performance of a conditional
discrimination task. Behav. Brain Res. 38, 243–261
29. Packard, M. G. & Knowlton, B. J. Learning and
memory functions of the basal ganglia. Annu. Rev.
Neurosci. 25, 563–593 (2002).
30. White, N. M. A functional hypothesis concerning the
striatal matrix and patches: mediation of S–R memory
and reward. Life Sci. 45, 1943–1957 (1989).
31. Packard, M. G. Glutamate infused posttraining into
the hippocampus or caudate-putamen differentially
strengthens place and response learning. Proc. Natl
Acad. Sci. USA 96, 12881–12886 (1999).
32. Packard, M. G. & McGaugh, J. L. Inactivation of
hippocampus or caudate nucleus with lidocaine
differentially affects expression of place and response
learning. Neurobiol. Learn. Mem. 65, 65–72 (1996).
33. Poldrack, R. A. & Packard, M. G. Competition among
multiple memory systems: converging evidence from
animal and human brain studies. Neuropsychologia
41, 245–251 (2003).
34. Bayley, P. J., Frascino, J. C. & Squire, L. R. Robust
habit learning in the absence of awareness and
independent of the medial temporal lobe. Nature 436,
35. Knowlton, B. J., Mangels, J. A. & Squire, L. R.
A neostriatal habit learning system in humans. Science
273, 1399–1402 (1996).
36. Moody, T. D., Bookheimer, S. Y., Vanek, Z. &
Knowlton, B. J. An implicit learning task activates
medial temporal lobe in patients with Parkinson’s
disease. Behav. Neurosci. 118, 438–442 (2004).
37. Kawagoe, R., Takikawa, Y. & Hikosaka, O. Expectation
of reward modulates cognitive signals in the basal
ganglia. Nature Neurosci. 1, 411–416 (1998).
38. Lauwereyns, J. et al. Feature-based anticipation of
cues that predict reward in monkey caudate nucleus.
Neuron 33, 463–473 (2002).
39. Lauwereyns, J., Watanabe, K., Coe, B. & Hikosaka, O.
A neural correlate of response bias in monkey caudate
nucleus. Nature 418, 413–417 (2002).
40. Pasupathy, A. & Miller, E. K. Different time courses of
learning-related activity in the prefrontal cortex and
striatum. Nature 433, 873–876 (2005).
41. Joel, D. & Weiner, I. The connections of the
dopaminergic system with the striatum in rats and
primates: an analysis with respect to the functional
and compartmental organization of the striatum.
Neuroscience 96, 451–474 (2000).
42. West, M. O. et al. A region in the dorsolateral striatum
of the rat exhibiting single-unit correlations with
specific locomotor limb movements. J. Neurophysiol.
64, 1233–1246 (1990).
43. Partridge, J. G., Tang, K. C. & Lovinger, D. M. Regional
and postnatal heterogeneity of activity-dependent
long-term changes in synaptic efficacy in the dorsal
striatum. J. Neurophysiol. 84, 1422–1429 (2000).
The first study to demonstrate regional variations
in the types and mechanisms of striatal synaptic
44. Whishaw, I. Q., Mittleman, G., Bunch, S. T. &
Dunnett, S. B. Impairments in the acquisition,
retention and selection of spatial navigation strategies
after medial caudate-putamen lesions in rats. Behav.
Brain Res. 24, 125–138 (1987).
45. Devan, B. D., McDonald, R. J. & White, N. M. Effects
of medial and lateral caudate-putamen lesions on
place- and cue-guided behaviors in the water maze:
relation to thigmotaxis. Behav. Brain Res. 100, 5–14
46. Devan, B. D. & White, N. M. Parallel information
processing in the dorsal striatum: relation to
hippocampal function. J. Neurosci. 19, 2789–2798
47. Yin, H. H., Knowlton, B. J. & Balleine, B. W.
Blockade of NMDA receptors in the dorsomedial
striatum prevents action–outcome learning in
instrumental conditioning. Eur. J. Neurosci. 22,
48. Yin, H. H., Ostlund, S. B., Knowlton, B. J. & Balleine,
B. W. The role of the dorsomedial striatum in
instrumental conditioning. Eur. J. Neurosci. 22,
49. Yin, H. H. & Knowlton, B. J. Contributions of striatal
subregions to place and response learning. Learn.
Mem. 11, 459–463 (2004).
References 47–49 present a series of studies that
established for the first time a dissociation
between S–R learning in the DLS and A–O learning
in the pDMS.
50. Ragozzino, M. E. Acetylcholine actions in the
dorsomedial striatum support the flexible shifting of
response patterns. Neurobiol. Learn. Mem. 80,
they can also be dissociated in terms of their underlying
neural substrates, in the form of distinct cortico-basal
Clearly, an understanding of network interactions
that result in a switch in behavioural control from
actions to habits has important implications for the study
of skill learning, addiction and various clinical disorders
resulting from basal ganglia abnormalities. At present,
however, we remain ignorant of the detailed mechanisms
that underlie habit formation at all levels of analysis. At
the behavioural level, all the conditions that promote
habit formation have yet to be characterized precisely.
Although several behavioural characteristics of habits
can be specified (for example, insensitivity to outcome
devaluation and contingency degradation, lack of behav-
ioural flexibility and lack of awareness in humans), other
characteristics are less clear (for example, the degree of
effector specificity and the need for attention during
learning). At the neural systems level, we do not yet
understand the properties of the cortico-basal ganglia
networks responsible for differences in behavioural
flexibility, or in sensitivity to instrumental contingency
manipulations. At the cellular level, in addition to our
ignorance of the detailed molecular mechanisms under-
lying synaptic transmission and plasticity in the basal
ganglia, we do not yet understand how synaptic plasticity
in the basal ganglia alters the outputs of the networks,
and we do not have direct evidence linking such plas-
ticity to well-defined learning. Nevertheless, we hope
that the framework proposed here will stimulate future
research, by directing attention to those variables that
are crucial in the analysis of purposive behaviour, and
by underscoring the importance of precise behavioural
analysis in elucidating the functions of neural systems.
NATURE REVIEWS | NEUROSCIENCE
VOLUME 7 | JUNE 2006 | 475
51. Ragozzino, M. E., Jih, J. & Tzavos, A. Involvement of
the dorsomedial striatum in behavioral flexibility: role
of muscarinic cholinergic receptors. Brain Res. 953,
52. Ragozzino, K. E., Leutgeb, S. & Mizumori, S. J. Dorsal
striatal head direction and hippocampal place
representations during spatial navigation. Exp. Brain
Res. 139, 372–376 (2001).
53. Mulder, A. B., Tabuchi, E. & Wiener, S. I. Neurons in
hippocampal afferent zones of rat striatum parse
routes into multi-pace segments during maze
navigation. Eur. J. Neurosci. 19, 1923–1932 (2004).
54. Delgado, M. R., Locke, H. M., Stenger, V. A. &
Fiez, J. A. Dorsal striatum responses to reward and
punishment: effects of valence and magnitude
manipulations. Cogn. Affect. Behav. Neurosci. 3,
55. Delgado, M. R., Stenger, V. A. & Fiez, J. A. Motivation-
dependent responses in the human caudate nucleus.
Cereb. Cortex 14, 1022–1030 (2004).
56. Zink, C. F., Pagnoni, G., Martin-Skurski, M. E.,
Chappelow, J. C. & Berns, G. S. Human striatal
responses to monetary reward depend on saliency.
Neuron 42, 509–517 (2004).
57. Tricomi, E. M., Delgado, M. R. & Fiez, J. A. Modulation
of caudate activity by action contingency. Neuron 41,
An interesting human imaging study that provided
strong evidence for the role of the caudate in
encoding A–O contingencies.
58. Williams, Z. M. & Eskandar, E. N. Selective
enhancement of associative learning by
microstimulation of the anterior caudate. Nature
Neurosci. 9, 562–568 (2006).
59. Dickinson, A., Balleine, B., Watt, A. & Gonzalez, F.
Motivational control after extended instrumental
training. Anim. Learn. Behav. 23, 197–206 (1995).
60. Balleine, B. W. & Dickinson, A. Goal-directed
instrumental action: contingency and incentive
learning and their cortical substrates.
Neuropharmacology 37, 407–419 (1998).
61. Corbit, L. H. & Balleine, B. W. The role of prelimbic
cortex in instrumental conditioning. Behav. Brain Res.
146, 145–157 (2003).
62. Leon, M. I. & Shadlen, M. N. Effect of expected reward
magnitude on the response of neurons in the
dorsolateral prefrontal cortex of the macaque. Neuron
24, 415–425 (1999).
63. Tsujimoto, S. & Sawaguchi, T. Properties of delay-
period neuronal activity in the primate prefrontal
cortex during memory- and sensory-guided saccade
tasks. Eur. J. Neurosci. 19, 447–457 (2004).
64. Tsujimoto, S. & Sawaguchi, T. Neuronal representation
of response–outcome in the primate prefrontal cortex.
Cereb. Cortex 14, 47–55 (2004).
65. Tsujimoto, S. & Sawaguchi, T. Working memory of
action: a comparative study of ability to selecting
response based on previous action in New World
monkeys (Saimiri sciureus and Callithrix jacchus).
Behav. Processes 58, 149–155 (2002).
66. Corbit, L. H., Muir, J. L. & Balleine, B. W. Lesions of
mediodorsal thalamus and anterior thalamic nuclei
produce dissociable effects on instrumental
conditioning in rats. Eur. J. Neurosci. 18, 1286–1294
67. Ostlund, S. B. & Balleine, B. W. Lesions of medial
prefrontal cortex disrupt the acquisition but not the
expression of goal-directed learning. J. Neurosci. 25,
68. Corbit, L. H., Ostlund, S. B. & Balleine, B. W.
Sensitivity to instrumental contingency degradation is
mediated by the entorhinal cortex and its efferents via
the dorsal hippocampus. J. Neurosci. 22,
69. Packard, M. G. & McGaugh, J. L. Double dissociation
of fornix and caudate nucleus lesions on acquisition of
two water maze tasks: further evidence for multiple
memory systems. Behav. Neurosci. 106, 439–446
70. Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel
organization of functionally segregated circuits linking
basal ganglia and cortex. Annu. Rev. Neurosci. 9,
71. Reep, R. L., Cheatwood, J. L. & Corwin, J. V. The
associative striatum: organization of cortical
projections to the dorsocentral striatum in rats.
J. Comp. Neurol. 467, 271–292 (2003).
72. Dalley, J. W., Cardinal, R. N. & Robbins, T. W.
Prefrontal executive and cognitive functions in
rodents: neural and neurochemical substrates.
Neurosci. Biobehav. Rev. 28, 771–784 (2004).
73. Divac, I., Markowitsch, H. J. & Pritzel, M. Behavioral
and anatomical consequences of small intrastriatal
injections of kainic acid in the rat. Brain Res. 151,
74. Levy, R., Friedman, H. R., Davachi, L. &
Goldman-Rakic, P. S. Differential activation of the
caudate nucleus in primates performing spatial and
nonspatial working memory tasks. J. Neurosci. 17,
75. Hassani, O. K., Cromwell, H. C. & Schultz, W. Influence
of expectation of different rewards on behavior-related
neuronal activity in the striatum. J. Neurophysiol. 85,
76. Kimura, M., Aosaki, T. & Ishida, A. Neurophysiological
aspects of the differential roles of the putamen and
caudate nucleus in voluntary movement. Adv. Neurol.
60, 62–70 (1993).
77. Kanazawa, I., Murata, M. & Kimura, M. Roles of
dopamine and its receptors in generation of choreic
movements. Adv. Neurol. 60, 107–112 (1993).
78. Joel, D. & Weiner, I. The organization of the basal
ganglia-thalamocortical circuits: open interconnected
rather than closed segregated. Neuroscience 63,
An important review in a series by the same
authors arguing for interactions between cortico-
basal ganglia networks.
79. Joel, D. & Weiner, I. The connections of the primate
subthalamic nucleus: indirect pathways and the
open-interconnected scheme of basal ganglia-
thalamocortical circuitry. Brain Res. Brain Res. Rev.
23, 62–78 (1997).
80. Haber, S. N., Fudge, J. L. & McFarland, N. R.
Striatonigrostriatal pathways in primates form an
ascending spiral from the shell to the dorsolateral
striatum. J. Neurosci. 20, 2369–2382 (2000).
81. Redgrave, P., Prescott, T. J. & Gurney, K. The basal
ganglia: a vertebrate solution to the selection
problem? Neuroscience 89, 1009–1023 (1999).
82. Haber, S. N. The primate basal ganglia: parallel and
integrative networks. J. Chem. Neuroanat. 26,
83. Middleton, F. A. & Strick, P. L. Basal ganglia and
cerebellar loops: motor and cognitive circuits. Brain
Res. Brain Res. Rev. 31, 236–250 (2000).
84. Rand, M. K. et al. Characteristics of sequential
movements during early learning period in monkeys.
Exp. Brain Res. 131, 293–304 (2000).
85. McGeorge, A. J. & Faull, R. L. The organization of the
projection from the cerebral cortex to the striatum in
the rat. Neuroscience 29, 503–537 (1989).
86. Jueptner, M., Frith, C. D., Brooks, D. J.,
Frackowiak, R. S. & Passingham, R. E. Anatomy of
motor learning. II. Subcortical structures and learning
by trial and error. J. Neurophysiol. 77, 1325–1337
87. Jueptner, M. et al. Anatomy of motor learning.
I. Frontal cortex and attention to action.
J. Neurophysiol. 77, 1313–1324 (1997).
88. Poldrack, R. A. et al. The neural correlates of motor
skill automaticity. J. Neurosci. 25, 5356–5364
References 85–88 show shifts in activation
patterns of cortico-basal ganglia networks in the
course of skill learning.
89. Daw, N. D., Niv, Y. & Dayan, P. Uncertainty-based
competition between prefrontal and dorsolateral
striatal systems for behavioral control. Nature
Neurosci. 8, 1704–1711 (2005).
90. Everitt, B. J. & Wolf, M. E. Psychomotor stimulant
addiction: a neural systems perspective. J. Neurosci.
22, 3312–3320 (2002).
91. Altman, J. et al. The biological, social and clinical
bases of drug addiction: commentary and debate.
Psychopharmacology (Berl.) 125, 285–345
92. Porrino, L. J., Lyons, D., Smith, H. R., Daunais, J. B. &
Nader, M. A. Cocaine self-administration produces a
progressive involvement of limbic, association, and
sensorimotor striatal domains. J. Neurosci. 24,
93. Williams, D. R. & Williams, H. Automaintenance in the
pigeon: sustained pecking despite contingent non-
reinforcement. J. Exp. Anal. Behav. 12, 511–520
94. Robinson, T. E. & Berridge, K. C. Addiction. Annu. Rev.
Psychol. 54, 25–53 (2003).
95. Berridge, K. C. & Robinson, T. E. What is the role of
dopamine in reward: hedonic impact, reward learning,
or incentive salience? Brain Res. Brain Res. Rev. 28,
96. Tiffany, S. T. A cognitive model of drug urges and drug-
use behavior: role of automatic and nonautomatic
processes. Psychol. Rev. 97, 147–168 (1990).
97. Rescorla, R. A. & Solomon, R. L. Two-process learning
theory: relationships between Pavlovian conditioning
and instrumental learning. Psychol. Rev. 74,
98. Corbit, L. H. & Balleine, B. W. Double dissociation of
basolateral and central amygdala lesions on the general
and outcome-specific forms of Pavlovian–instrumental
transfer. J. Neurosci. 25, 962–970 (2005).
99. Holland, P. C. Relations between Pavlovian–
instrumental transfer and reinforcer devaluation.
J. Exp. Psychol. Anim. Behav. Process. 30, 104–117
100. Corbit, L. H., Muir, J. L. & Balleine, B. W. The role of
the nucleus accumbens in instrumental conditioning:
evidence of a functional dissociation between
accumbens core and shell. J. Neurosci. 21,
101. Canales, J. J. & Graybiel, A. M. A measure of striatal
function predicts motor stereotypy. Nature Neurosci.
3, 377–383 (2000).
102. Rhodes, S. E. & Killcross, S. Lesions of rat infralimbic
cortex enhance recovery and reinstatement of an
appetitive Pavlovian response. Learn. Mem. 11,
103. Coutureau, E. & Killcross, S. Inactivation of the
infralimbic prefrontal cortex reinstates goal-directed
responding in overtrained rats. Behav. Brain Res. 146,
104. Killcross, S. & Coutureau, E. Coordination of actions
and habits in the medial prefrontal cortex of rats.
Cereb. Cortex 13, 400–408 (2003).
105. Everitt, B. J. & Robbins, T. W. Neural systems of
reinforcement for drug addiction: from actions to
habits to compulsion. Nature Neurosci. 8,
106. Baum, W. M. The correlation-based law of effect.
J. Exp. Anal. Behav. 20, 137–153 (1973).
107. Dickinson, A. Actions and habits: the development of
behavioural autonomy. Phil. Trans. R. Soc. Lond. B
308, 67–78 (1985).
108. Kerr, J. N. & Wickens, J. R. Dopamine D-1/D-5
receptor activation is required for long-term
potentiation in the rat neostriatum in vitro.
J. Neurophysiol. 85, 117–124 (2001).
109. Reynolds, J. N., Hyland, B. I. & Wickens, J. R.
A cellular mechanism of reward-related learning.
Nature 413, 67–70 (2001).
110. Gerdeman, G. L., Partridge, J. G., Lupica, C. R. &
Lovinger, D. M. It could be habit forming: drugs of
abuse and striatal synaptic plasticity. Trends Neurosci.
26, 184–192 (2003).
111. Gerdeman, G. L., Ronesi, J. & Lovinger, D. M.
Postsynaptic endocannabinoid release is critical to
long-term depression in the striatum. Nature
Neurosci. 5, 446–451 (2002).
112. Packard, M. G. & White, N. M. Dissociation of
hippocampus and caudate nucleus memory systems
by posttraining intracerebral injection of dopamine
agonists. Behav. Neurosci. 105, 295–306 (1991).
113. Sage, J. R. & Knowlton, B. J. Effects of US devaluation
on win-stay and win-shift radial maze performance in
rats. Behav. Neurosci. 114, 295–306 (2000).
114. Packard, M. G., Hirsh, R. & White, N. M. Differential
effects of fornix and caudate nucleus lesions on two
radial maze tasks: evidence for multiple memory
systems. J. Neurosci. 9, 1465–1472 (1989).
H.H.Y. was supported by the Intramural Research Program
at the National Institute on Alcohol Abuse and Alcoholism,
National Institutes of Health. B.J.K. was supported by a
National Science Foundation grant. We would like to thank
B. Balleine, R. Costa, N. Daw, T. Dickinson and S. Ostlund
for helpful discussion.
Competing interests statement
The authors declare no competing financial interests.
The following terms in this article are linked online to:
Knowlton’s homepage: http://www.psych.ucla.edu/Faculty/
Access to this links box is available online.
476 | JUNE 2006 | VOLUME 7