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Behaviorism, Cognitivism and the Neuropsychology of Memory

Author(s): Herbert L. Petri and Mortimer Mishkin
Source: American Scientist, Vol. 82, No. 1 (January-February 1994), pp. 30-37
Published by: Sigma Xi, The Scientific Research Society
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Behaviorism,
Cognitivism
Neuropsychology
Is learninga matterofbehavioralpatterningby reinforcement,
or thestorage
and use ofknowledge?A model ofhow thebrainremembers supportsbothviews
Herbert L. Petri and Mortimer Mishkin
is a remarkable ability that
Learningis shared by all animals. But it is
not a simple thing to understand. The
question ofwhat we learn, for instance,
is one of themost elusive in the history
of modern psychology. And it lies at
the core of one of the longest-running
controversies in the field.
The controversy has split along the
two lines of thought called behavior?
ism and cognitivism. Behaviorism ap?
peared around the turn of the century
and reigned until around 1960. The
early behaviorists viewed learning as
automatic and machinelike, beyond
the awareness of even themost aware
organism. They observed that ifa par?
ticular response to a particular stimu?
lus pays off for an organism, the re?
sponse is likely to be repeated, and the
probability that the response will be
further repeated will be increased by
continued rewards.
This view of learning, however, was
criticized by some who believed that
higher organisms, at least, could develop
expectations. The newer view, cogni
Herbert L. Petri is professor of psychology at
Towson State University and adjunct professor of
psychology at The JohnsHopkins University, where
he earned his Ph.D. He is theauthor ofMotivation:
Theory, Research and Applications,
now in its
third edition.Mortimer Mishkin, who received his
Ph.D. fromMcGill University, isChief of the
Laboratory ofNeuropsychology at theNational
Institute ofMental Health, where he has conducted
research since 1955. A past president of theSociety
forNeuroscience, he serves on the editorial board of
15 journals and is the recipient of numerous inter?
national awards and honors. He continues topub?
lish extensively in the area of brain mechanisms
and behavior. Address for Petri: Department of
Psychology, Towson State University, Towson,
MD 21204-7097.
30 American Scientist, Volume 82
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and
of
Memory
tivism, held that individuals can acquire
and store information that can be com?
bined with new information to lead to
new types of behavior. The novel solu?
tions canmaterialize rapidly,without the
need forrepeated response to a stimulus.
The cognitive perspective now
dominates ideas on learning and
memory in the field of psychology,
without replacing much of what be?
haviorism has provided. As some?
times happens in science, a paradigm
shift has led away from earlier ideas
without refuting those ideas. Both
views about how behavior is learned
and retained have empirical support.
But they are very different, and it is
difficult to imagine how to develop a
theory of learningwithout deciding on
one model or the other.
Or is itpossible that there is a way in
which behaviorism and cognitivism
might complement each other? It now
appears that there is.As experimental
psychologists have labored over the
years to testmodes of learning in peo?
ple and animals, neuropsychologists
have been studying the neural systems
thatprocess and store information.The
upshot ofmuch of this research is that
thebrain appears to contain more than
one system for learning and retention.
From neuropsychological experiments
has arisen a dual-system theory of
learning, with important implications
for future research and application. It
turns out that these experiments sup?
port both the behaviorist and cogni
tivist approaches by suggesting that
each is consistent with a different
mechanism and a different neural sys?
tem. Furthermore, the mammalian
brain, at least, appears to have both
mechanisms. We probably learn both
All use subject to JSTOR Terms and Conditions
the
ways. The two different theories may
have arisen, inpart, to explain different
experimental results generated by the
greater activation of one learning sys?
tem or the other. And what we learn
probably depends on how much each
system is activated during learning.
Studies of Learning
The systematic study of learning began
in the 1890s,with Edward L. Thorndike's
observations of cats confined to puzzle
boxes. The hungry cats, tryingto escape,
would hit upon a correct solution after a
time. Rewarded by food, they took less
and less time to find theirway out as
the trialswere repeated. In a remark?
able doctoral thesis published in 1898,
Thorndike formulated what he called
the "law of effect."He suggested that
behavior begins as essentially random
activity, but connections are strength?
ened between stimuli and responses
when those responses are followed by
some satisfying state of affairs. This set
of links involving stimulus, response
and consequence was the precursor of
what inmodern usage is known as re?
inforcement.Thorndike thus offered a
psychological analogue to the evolu?
tionary law of natural selection that
Charles Darwin had proposed a quar?
ter-century earlier. In Darwin's
theory,
random mutation produces traits that
can be adaptive (successful) or non
adaptive in a given environment, de?
termining the chances that an organ?
ism and its offspring will survive.
Thorndike's cats repeated thebehavior
that turned out, like some mutations,
to be adaptive.
Beginning in the 1930s, the best
known behaviorist, B. E Skinner, re?
fined Thorndike's ideas. Skinner de
 I ''''^ '
\|- '^^^^mxtf^^M

or memories?
Figure 1.What is it that we learn?habits Behaviorist theory emphasizes ways of learning that are automatic and machinelike,
whereas cognitivists believe the primate brain stores information, makes associations and uses insight from past experience in devising new
behavioral solutions. Recent neuropsychological research supports the view that the brain has two systems for learning. Habit-based learning
(from taking up smoking tomastering a complex on the can take or cognitive, (as is re?
piece piano) place alongside memory-based, learning
for card-playing). What is learned may depend on whether the habit system or the memory
quired system is activated during learning. Often
the two systems are simultaneously active, as in this scene from the 1961 film "The Hustler," with Paul Newman and George C. Scott. (Photo?

graph courtesy of the Museum of Modern Art Film Stills Archive.)

emphasized the importance of the con?
nection between a stimulus and its re?
sponse and stressed instead the idea
that reinforcement strengthens a re?
sponse, making itmore probable. Skin?
ner's ideas were corroborated by care?
ful experimentation, and today they
are an integral part of the
psychology
of learning.
Another contribution to behaviorist
thought was made in 1943 by Clark L.
Hull, who attempted to devise a theory
that would include the major factors
that interacted to produce behavior. who in 1932 argued for the importance
One such factorwas habit, Hull's term of goals, expectancies and purpose.
for learning. Hull considered habits to Tolman proposed that organisms learn
be stimulus-response pairs that were thatparticular responses lead to partic?
strengthened by reinforcement. He as? ular goals; they retain information, and
sumed that an animal acquires habits that information is confirmed, or not,
as each reinforced
gradually, pairing of by experience, resulting in learning.
stimulus and response adds a small in? The role of reinforcement therefore is
crement to the probability that a par? not to change the probability of a given
ticular behavior will happen. response, but to lead to the develop?
The behaviorist view was not uni? ment of expectancies about how cer?
versally accepted. Notable among its tain goals can be reached.
early detractors was Edward Tolman, Another early cognitivist, Wolfgang

1994 January-February 31

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K?hler, set out on a slightly different The work of Tolman, K?hler and has focused attention on novel behav?
track in search of original and complex Krechevsky showed that learning does ior: If new information can be com?
forms of learning in primates; his re? not have to be automatic and without bined in various ways with informa?
sults, published in 1925, appeared to awareness; at least in some cases, it ap? tion already acquired, then new types
show that the learning of some of his pears to be quite purposeful. The evi? of behavior are possible. Insight can
chimpanzees was guided by insight, dence of purposeful behavior suggests lead to novel behavioral solutions.
the discovery of relations among bits that animals and people have an Such solutions are thought to happen
of stored information. In a similar vein, awareness of what is being acquired rapidly, in as little as one exposure.
I. Krechevsky proposed in 1938 that and that they actively interpret the Itwas hard to imagine a meeting
animals as well as people are capable stimuli they sense from the environ? ground forbehaviorist and cognitivist
of testing hypotheses. ment. The popularity of cognitivism theories of learning. Finding such a
synthesis required a different perspec?
tive, a step back from the apparently
conflicting results of the great experi?
mentalists. As we have mentioned, the
field of neuropsychology offers such a
perspective. Neuropsychological re?
search has shown that theremust be
more than one system in the brain in?
volved in the acquisition and retention
of experience.
We have proposed a two-system
model, separating the system that stores
(cognitive) memories from another sys?
tem involved in developing (noncogni
tive) habits. It is not a coincidence that
these are the terms commonly used by
' ~ cognitivists, on the one hand, and be
?rr haviorists, on the other, to describe the
,-?i respective products of the type of learn?
ing that each studies. Memories are
stored information that is available to
cognition?that is, information that can
be known. A habit system, by contrast,
would store learned behavior that isnot
necessarily available to cognition. (Al?
though the dual-systems model has
been developed primarily as a result of
research with monkeys, it is assumed
that the relevant structures in the hu?
man brain are homologous to those in
themonkey brain.)
Neuropsychologists have devised
various terms to describe this split be?
tween retention systems. Larry R.
Squire, of theUniversity of California
at San Diego (UCSD), uses the terms
declarative formemories and nondeclar
ative for habits as well as for other
types of noncognitive learning (such as
repetition priming). Peter Graf and
^^^^^^^
?^B^^l^l^l^B^ Daniel Schacter at the University of
Figure 2. Distinguishing between familiar objects requires the use of recogni?
and unfamiliar Toronto have suggested the terms ex?
plicit and implicitmemory for thisma?
tion memory. Experiments with monkeys in author Mortimer Mishkin's laboratory at the Na?
tional Institute ofMental Health in 1978 established that the bilateral removal of structures in
jor distinction between systems. (In?
the medial temporal lobe of the brain (the hippocampus, the amygdala and the underlying rhi
nal cortex) disrupted the monkeys'
vestigators are currently subdividing
ability to recognize objects and form associations. To obtain
each of these major divisions into
a reward (such as a raisin or peanut) in a task called delayed nonmatching to sample, a monkey
many more.) We begin with what is
must push aside a three-dimensional object placed over a central food well (top). After a delay,
the monkey is confronted with two objects, the original and a new one, each covering a later?
known about the cognitive memory
al food well. The monkey must choose the new object (bottom). When required to recognize system, because themethodology of
one object as familiar, monkeys with lesions of the medial
temporal lobe displayed the amne? neuropsychology has been most suc?
sia often observed in human patients with damage to the same part of the brain. (Photographs cessful in describing the brain struc?
by Elisabeth Murray; provided by Jocelyne Bachevalier.) tures associated with this system.

32 American Scientist, Volume 82

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Memory And the Brain
Memory, the ability to store sensory in?
formation for later retrieval as images,
thoughts and ideas, is an obvious re?
quirement for learning in the cogni
tivistmodel. A cognitive memory sys?
tem would logically be made up of
stored neural representations of stimuli
that can be first recognized and then
connected to create associations. Is / n (foreran
^/ /^^^BNSSK^^ ^\ \ / ^^?
there such a store in the brain, and if
so, what are themechanisms for stor?
ing and retrieving information? Much
effort has gone into answering these
questions and identifying what parts
of the brain are involved.
Neuroscientists often learn what
part of the brain is associated with a
particular function by studying the ef?
fects of localized brain damage. Many
investigators have studied closely the
phenomenon of amnesia inhuman pa?
tients and monkeys in thisway, by as? Figure 3.Memory-system structures and pathways have been established by experiments (such as
that shown in Figure 2) that assess memory
certaining the exact location of brain le? impairment in individuals with damage to key areas
of the brain. The memory model posits that information from past experience is stored in locations
sions and associating the lesions with
where it can be reactivated by sensory input and associated with new It has been de?
the patients' specific memory deficits. experience.
on the basis of research on the
The story of a famous patient known veloped monkey brain. A human brain is shown here. The rhinal
cortex underlying the amygdala and hippocampus appears to be crucial for recognition memory.
as H. M., first told in the 1950s byWil? Connections from these structures in themedial temporal lobe go to the thalamus and themarnil
liam Scoville and Brenda Milner, fasci? located near the center of the brain. The medial thalamus sends neural fibers (not
lary bodies,
nated neuropsychologists and provid? shown) to the ventromedial prefrontal cortex, which in turn sends fibers back to the rhinal cortex
ed important insight into the brain and to the basal forebrain. The basal forebrain also receives fibers from the medial temporal
structures involved with certain kinds lobe. The basalforebrain projects to the highest-order sensory area (among others), closing the
of
learning
and memory. H. M.'s se? loop that appears necessary for the storage of sensory experiences.
vere epilepsy had been treated
by
surgery that damaged themedial part
of the temporal lobe in both hemi?
spheres. The result was a type of am?
nesia; H. M. retained many memories
and intellectual abilities, but he seemed
areas areas * areas $
incapable of forming new memories. I sensory sensory prefrorrtal
This phenomenon is called anterograde ||Bb
amnesia because itdoes not destroy old
memories, but blocks learning (the ac?
quisition of new memories).
Efforts to develop neural models of
memory based on animal research suf?
fered formany years from the inabilityof
investigators to produce in animals the
same global anterograde amnesia ob?
served inhuman patients such as H. M.
The difficultycame about because inves?
tigators had focused almost exclusively
on thehippocampus as the likely struc?
ture that, when damaged, produced Figure 4.Memory system's feedback loops are thought to operate as shown here. Sensory input
the amnesia, and this focus affected the arriving in the higher-order sensory areas of the cerebral cortex triggers structures in the medi?
al temporal lobe concerned with recognition memory and associative (Current re?
choice of tests used to assess amnesia memory.
search suggests that the rhinal cortex within themedial temporal lobe is necessary for recogni?
in animals. But in 1978 one of us
tion memory.) The temporal-lobe structures activate structures in the medial thalamus. The
(Mishkin) found that this form of am? medial thalamus, in turn, activates ventromedial areas in the prefrontal cortex. The medial tem?
nesia could be created by the bilateral
poral lobe and ventromedial prefrontal cortex also extend neural projections to the basal fore
removal of the same structures re?
brain, which has connections that feed back to the medial-temporal and sensory areas. The
moved in H. M. (the hippocampus, model that the storage of stimulus memories
presumes requires the activation of these loops
amygdala and underlying cortex) and and the feedback produced by the cholinergic cells in the basal forebrain (those that communi?
then examining themonkeys in a task cate using the neurotransmitter acetylcholine) onto the higher-order sensory areas.

1994 January-February 33

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 to themedial temporal lobe. It appears,
then, that one can identify a memory
pathway in thebrain. Sensory informa?
tion is processed by the appropriate
primary sensory cortices?the areas of
the brain that receive direct sensory in?

A-B ? B3B put?and it is passed stage by stage to

the areas of the cortex that further
process the information and form the
basis of perception. The final process?
ing stations for sensory information ac?
tivate the rhinal cortex, which in turn
stimulates thalamic target nuclei and
the frontal cortex through the path?
ways just described. These three struc?
tures form a part of the so-called limbic
system (the medially located ring of
cerebral tissue surrounding the dien
cephalon and the brainstem).
The medial thalamus and orbital cor?
Figure 5.What a person typically calls may be the result of changes in the activity
knowledge tex provide a feedback loop through
of cells in the cerebral cortex as a result of experience. Robert Desimone has outlined four ways
the rhinal cortex to the final sensory
inwhich neuronal activity is altered during the formation or expression of memory traces: tun?
processing stations. In addition, there
ing, adaptive filtering, sustained activation and association. (From Desimone 1992.)
appears to be a second feedback loop
from the limbic system to the basal
involving visual recognition of an ob? Among the parts of the diencephalon forebrain system (a region at thebase of
ject. The task, called delayed non implicated in amnesia are themedial the cerebrum), which, through the
matching to sample, requires a mon? portion of the large structure called the chemical signaling system that involves
key to choose the unfamiliar object in a thalamus and the small structures theneurotransmitter acetyldioline, also
pair, the other object having been called mamillary bodies. In studies in feeds back to the final sensory process?
shown only once, for familiarization, a 1983 at NIMH, JohnAggleton found ing station. This activation of the high?
minute or two earlier. Monkeys with that damage to the medial thalamus est-order sensory processing stations of
bilateral lesions could not distinguish also caused monkeys to fail a single the cortex by feedback is presumed to
between the unfamiliar and the famil? trial object-recognition test that is sen? be necessary for storage of the repre?
iar object in the pair. The impairment sitive to memory disruption. This sentation in the sensory area.
was later found by Elisabeth Murray was soon confirmed Zola The contents of this store in the cortex
finding by
to extend to recognition involving Morgan and his colleagues. are thought to be neural representations
touch as well as sight; further studies To understand how information is of the objects or events that triggered the
byMurray and others inMishkin's lab? processed in the brain, it is important circuit.A neural representation,when re?
oratory at the National Institute of not only to locate important structures activated at a later time, could then pro?
Mental Health (NIMH) showed that but also to trace the connections be? vide the basis for recognition memory.
the surgery disrupted the monkeys' tween them. The rhinal cortex men? One can imagine thata sensorymessage
ability to form associations between tioned above is known to extend nerve might travel along these pathways until
stimuli, as well as their ability to recog? fibers to the same nuclei (groups of cell it reached amatching representation.
nize stimuli. bodies) within themedial thalamus that The memory system seems capable
Initially itappeared that the damage were damaged in the amnesic monkeys. of storing a neural representation in
responsible for the anterograde amne? Fibers also extend to the orbital pre as little as one exposure. Furthermore,
sia was the combined destruction of frontal cortex (a portion of the frontal it seems likely that representations be?
the amygdala and the hippocampus. lobe), and damage to this area also was come linked to one another by associ?
Later, serious questions arose about shown by Jocelyne Bachevalier (now at ation. Such associations between rep?
this idea. Recent results from studies in theUniversity of Texas Health Sciences resentations appear to be formed
this laboratory, and the laboratories of Center inHouston) and Mishkin topro? indirectly through the structures iden?
James Horel at Syracuse University duce amnesia inmonkeys. The latter tified above. These neural representa?
and Stuart Zola-Morgan atUCSD, now two structures are directly connected. tions and their associations thus offer
point to damage or dysfunction of the Thus it seems that circuits connecting the likely physical basis for the cogni
cortex underlying the hippocampus the rhinal cortex to those in the dien? tivist's concept of information or
and amygdala?especially the perirhi cephalon and the frontal lobe provide knowledge, and the previously de?
nal and entorhinal areas?as the cause pathways crucial for learning. Damage scribed feedback loops could provide
of the amnesia. to these pathways precludes the storage the circuitry underlying cognition.
Human amnesia can also result from of memory. Robert Desimone, an investigator at
damage to neural structures in other Neuropsychologists and neuro NIMH, summarized his and others'
areas, inparticular the diencephalon, a anatomists have also traced pathways findings on single-neuron recordings
region at the very center of the brain. thatwould carry sensory information in a 1992 review. Neurons, Desimone

34 American Scientist, Volume 82

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wrote, can be tuned by perceptual ex?
perience to respond to a shape or other
sensation; they can undergo adaptivefil?
tering (Miller, Li and Desimone 1991),
inwhich they use stored information
to filternew information for similari?
ties; they can undergo sustained activa?
tion (see also Fuster and Jervey 1981;
Goldman-Rakic, Funahashi and Bruce
1990), providing a mechanism for pallidus
^V^glob|us ^^^^^^^^^W^^^^^l^ \ \ \y ^|
working memory; or they can be en?
gaged in association, the pairing of dif?
ferent stimuli (Mihashita 1988). What
we have called a stored neural repre? ?
nucleus
sentation may be a combination of the ^B^caud2e / //*?
processes described by Desimone. ^_AT ^V^H^^^^HmP nu<feus
^^sd^B
The Noncognitive Habit System
In a variety of studies startingwith the
study ofH. M., a curious phenomenon
was noted in patients with global an
terograde amnesia: They can still learn
and retain certain tasks, even afterdam? Figure 6. Major structures thought to be associated with the
development of habits are large?

age to themedial temporal lobe. (Alan ly distinct from those involved in memory formation. Activity in the visual areas of the

Parkin, then at theUniversity of Sussex temporal lobe (and other sensory areas) stimulates cells in the striatum, specifically the cau?
in England, in 1982 provided an excel? dal (tail) portion of the caudate nucleus and putamen. These areas in turn activate the
globus
and the pars reticulata of the substantia
lent review ofmuch of this earlier litera? pallidus nigra in the brainstem, which project to the
ventral portions of the thalamus. Cells within the ventral thalamus project to the premotor
ture.)The discovery, inpatients who are and supplementary motor portions of the frontal cortex.
otherwise amnesic, of a retained ability
to learn some types of taskswas a part
of the evidence that led researchers to
the conclusion thatmore than one re?
tention systemmust be present. As not?
ed earlier,we have termed a second set
of structures the habit system.
There is still relatively littleevidence
concerning the neural circuitry and the
structures thatmediate habit formation.
What evidence is available points to a
part of the brain called the extrapyra
midal system. A major part of this sys?
tem lies at the center of the forebrain
and is involved in motor functions
through connections with the premotor
cortex of the frontal lobe. Specifically,
the evidence identifies thebasal ganglia,
containing the caudate nucleus, puta
men and
globus pallidus, among other
structures, as part of the habit circuitry.
Figure 6 shows these structures.
Among the circuits that appear im?
portant for the conditioning of habits in
human beings are those that link the
cortex, the striatum (the caudate nucle?
us and putamen, parts of thebasal gan? Figure 7. Habit system appears to be activated by sensory input directed from the various
systems to the caudal portion of the caudate nucleus
glia) and themotor-cortex areas. In one sensory processing and to the putamen.
Activation of these cells, along with input from dopamine-producing cells in the pars com
of the first studies to show this,
pacta, part of the substantia nigra, is thought to strengthen connections.
Maryann Martone and her colleagues
stimulus-response
These connections are then evidenced in behavior as a result of the activation of
at the Boston University School ofMed? sequential
other structures shown in Figure 6: the globus and substantia nigra (pars reticulata),
pallidus
icine discovered in 1984 that patients and cells in the ventral thalamus and
(lower) the premotor and supplementary motor areas of
suffering from Huntingtons chorea the frontal cortex. The contents of the brain's habit "store" are thought to be response proba?
(the degenerative disorder character? bilities, rather than neural representations of objects or events; such
probabilities can be
ized by spasms of the face and extremi strengthened by reinforcement.

1994 35
January-February

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 ties), with known dysfunction of the
striatum, are
impaired
on a mirror
reading task.Amnesics are unimpaired
on the same task because of itshabitual
nature. Conversely, Huntington's pa?
tientsare unimpaired on a verbal recog?
nition task (requiring memory) that
amnesics fail. In 1993, in a review of
studies since theMartone et al. discov?
ery,William Heindel and his colleagues
at theUniversity of California School of
Medicine surveyed the selective deficits
shown by Huntington's patients and
concluded that there is substantial sup?
port for the role of corticostriatal cir?
cuits in the learning ofmotor skills and
central motor programs.
This combination of retention and
forgetting in amnesic patients has a par?
allel in the animal literature.One line of
research has shown that even though
monkeys with medial-temporal-lobe le?
sions show rapid forgetting in one-trial
object-recognition tasks, theyneverthe?
less are able to learn object discrimina?
tions, thought to be a type of habit for?
mation, when the same objects are
presented repeatedly. Furthermore, the
trials do not have to be repeated very
rapidly. Barbara Malamut, Richard
Saunders and Mishkin, presenting
work done at NIMH, showed in 1984
thatmonkeys with medial-temporal
damage learn object discriminations as
quickly as control animals do, even
when the interval between trials is as
long as 24 hours. Similarly, monkeys
with medial-diencephalic lesions are
impaired on object-recognition tasks but
learn visual discriminations as quickly
as control monkeys. A second set of
studies by Zola-Morgan and Squire in
1984 showed that the learning ofmotor
and perceptual skills is uriimpaired in
monkeys with large medial-temporal
lobe lesions.
Moreover, JinWang, Thomas Aigner
andMishkin, inwork also done atNIMH,
showed in 1990 that lesions of the cells in
the tail of the caudate and in the ventral
putamen impaired monkeys' perfor?
mance on thediscrimination-learning test
(a task requiring the development of a
habit) with 24-hour intertrialintervalsbut
not on the limbic-dependent object
recognition task,which calls upon cog?
nitive memory. In recent studiesin Nor?
man White's laboratory at McGill
University and in James McGaugh's
laboratory at theUniversity of Califor?
nia at Irvine,Mark Packard has found
evidence in rats that supports the dual
systems model noted here and shows
36 American Scientist, Volume 82
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the importance of the caudate nucleus
inparticular inhabit learning.
The learning of habits may seem
more primitive than cognitive memory,
but the underlying circuitry is not nec?
essarily simpler. Several lines of re?
search suggest that different learning
situations may lead by different circuit?
ry to habit formation, and habits may
be "stored" inmore than one part of
the brain. The kind of habit learning
treated so far is often referred to as in?
strumental conditioning. But habits
may also be formed by so-called classi?
cal or Pavlovian conditioning. (In clas?
sical conditioning an automatic or in?
voluntary response is provoked by a
neutral stimulus that has been paired
with a biologically significant, uncon?
ditioned stimulus; in thisway Pavlov's
a sound or
dogs came to salivate to
light that had been paired with food.)
For classical conditioning of somatic
responses, such as the blink of an eye,
circuits through the cerebellum are es?
sential, as was firstshown by Richard
Thompson and his colleagues at Stan?
fordUniversity. For classical condition?
ing of autonomic responses, such as
changes in heart rate, circuits through
the amygdala are critical (see, for ex?
ample, Kapp et al. 1982).
The question of what is stored in a
habit system is important. It is not the
cortical representation of stimulus
events and their associations, as it
would have to be in a cognitive memo?
ry system. Instead it is the probability
that a stimulus will elicit a response, a
probability that isdetermined by previ?
ously reinforced pairings. The locus of
the store is likely to be a subcortical
structure, including those referred to
above. Furthermore, if the structure is
the striatum, the neurotransmitter
dopamine, known to be important for
striatal function, is likely tobe the chem?
ical signaling system that triggers the
formation of thebond.
The product of habit learning is as?
sumed to be a stimulus-response bond
not accessible to conscious experience; it
is only a tendency to respond in a par?
ticularway in a particular situation. The
characteristics of a stimulus are capable
of triggering a response even though
those characteristics need not be recog?
nized?that is to say, no awareness is re?
quired. Further, itappears that response
a
probabilities develop gradually as re?
sult of repeated exposures, with each
exposure incrementally changing the
stored response probability.
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Robert A. Rescorla of theUniversity
of Pennsylvania showed in 1987 that the
associations that are observed as a re?
sult of irtstrumentalconditioning can be
made between a response and its rein
forcer (a reward, such as food, or a
penalty), between the stimulus and the
response, and perhaps between the
stimulus and the reinforcer. Rescorla's
research describes different types of as?
sociations thatwe suggest aremediated
by different learning-and-retention sys?
tems.According to themodel outlined
here, the stimulus-reinforcer association
would be mediated by thememory sys?
tem, and the
stimulus-response
associa?
tion would be mediated by the habit
system. The
response-reinforcer
associ?
ation would be mediated by either the
habit system or thememory system, de?
pending on thenature of the task.
Memories, Habits and Learning
The controversy over what is learned
may be themost fundamental contro?
versy within psychology. We propose
thatwhat is learned may depend on
how it is learned, and thatdifferent sys?
tems allow fordifferent kinds of learn?
ing. That there are functionally inde?
pendent retention systems is strongly
suggested by neuropsychology studies.
The dual-systems model, which is
meant to apply to themajor division be?
tween systems,proposes that the acquisi?
tion and retentionof the effectsof experi?
ence are best understood as resulting from
the action of two fundamentally different
learningand retentionsystems.These sys?
tems use different circuitrywithin the
brain, storedifferentaspects of experience
and follow differentrules of storage.
Access to the information within
these two systemswould also appear to
differ dramatically: The contents of the
habit system, although evident in be?
havior, appear often to be unavailable
to conscious awareness, whereas the
contents of the memory system are
readily available to conscious awareness
and are, thus,more easily manipulated
to formnew and novel associations.
The model suggests thatone does not
have to choose between behaviorist and
ex?
cognitivist explanations. Behaviorist
to most close?
planations appear parallel
ly the learning processes utilized by the
habit system,whereas cognitive expla?
nations parallel most closely those
processes active in thememory system.
The experimental paradigms used in the
study of learning,however, could be ex?
pected to activate both the habit and
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stances. The experiences encountered in long-term memory
a learning situation would be retained temporal cortex. Nature 335:817. memory systems by posttraining intracere?
Miller, E. K., L. Li and R. Desimone. 1991. A bral injection of dopamine agonists. Behav?
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Mishkin, M. 1993. Cerebral memory circuits. In Scoville, W B., and B. Milner. 1957. Loss of re?
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1994 January-February 37

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