human memory and the medial temporal region of the brain.pdf
TRANSCRIPT
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Short i t le
M MORY
ND THE
MEDI L TEMPOR L REGION
OF THE
BR IN
y
hilip M orsi
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HUM N MEMORY
ND THE MEDIAL TEMPORAL REGION OF THE BRAIN
y
Philip
M
Corsi
A thesis submitted
to
the
Faculty
of Graduate
Studies
and Reseal\cn
in
p r t i l
fulfilment of
the requirements
for
the
degree
of
Doctor
of
Philosophy.
e p ~ r t m e n t
of
Psychology
McGill University
Montreal April 26 972
Philip M
Corsi
973
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Ph.D.
Psychology
Phil ip M
Corsi
HUM N MEMORY
ND THE
MEDIAL TEMPORAL REGION
OF THE BRAIN
A clear
double
dissociat ion between the effects of l e f t
and
r igh t temporal-lobe
excisions
was demonstrated
for two
identically-designed learning
tasks
tha t u t i l ized
di f fe ren t
memoranda. Patients
with l e f t temporal-lobe
les ions
showed a
def i c i t for the
verbal
task and normal performance for the
non-verbal analogue,
whereas
the converse
was
evident for
pat ients with r ight temporal-lobe les ions. Again,
on
two
formally similar t e s t s
of short- term
r eca l l with in terpolated
act iv i ty th i s same pat tern of dissociat ion
was
observed for
the
re tent ion
of
verbal
as compared with
non-verbal information.
For
both pairs of experiments, the severi ty of the materia l
speci f ic learning and re tent ion def ic i t s was direc t ly re la ted
to the
extent
of
surgical encroachment
upon the
hippocampal
zone of the affected hemisphere. These studies implicate
the
hippocampal region in the crucia l t rans fe r of
experience
from a
temporary
storage system primary memory to more
permanent
long-term
storage
secondary memory).
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Preface
The chief finding here is tha t the medial temporal region
of the
brain
including the hippocampus and parahippocampal
gyrus is
vi ta l
for
several
aspects
of
human
learning.
In
par t icu la r , with
uni lateral
l e f t temporal lobectomy in
the
dominant hemisphere
for
speech the learning and
re tent ion
of
elementary
verbal information l e t te rs and numbers> is impaired.
I f the
l e f t
medial temporal region i s also excised then the
verbal memory defect is exacerbated. Yet the
re tent ion
of
non-verbal
information
such
as
spat ia l locat ion and spat ia l
sequence remains
in tac t .
Conversely af ter
surgical removal
of the
r igh t
temporal
lobe
the
learning and re tent ion
of
spat ia l locat ion
and
sequence
-
tasks
which
normally are
mediated without verbal s tra tegies -
are more
di f f i cu l t ,
although the
reca l l of simple verbal elements proceeds
nor
mally. The severi ty
of th is
mater ia l -specif ic memory impair
ment
is direc t ly
related to
the
extent of
surgical encroachment
upon
the
hippocampal
zone
in
the
r igh t ,
nondominant
hemisphere.
With bi la te ra l damage to the medial temporal region a more
global memory disturbance resul t s . Although the anterograde
amnesia i s not complete t i s
emergent
with respect
to
the
memory defects observed a f te r
l e f t
and r igh t hippocampectomy.
I m
indebted to
the
pat ients
~ the Montreal
Neurological
Ins t i tu te
who
permitted
me
to
perform
these
studies
of
them.
I m
grateful to Dr. Theodore Rasmussen Dr.
Charles
Branch
and Dr.
William
Feindel
for
referr ing
the i r
pat ients to me.
Special thanks are offered
to
Miss Marcelle
Provencher
who
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with
great
patience and
care
transformed y handwrit ten
dr f t in to th i s f inished manuscript.
This work
was
supported by the
Medical
Research Council
of
Canada through Grant
M 2624
to
Dr. Brenda
Milner.
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Table
of
Contents
Introduction
1
The
Present
Invest igat ion
8
Subjects 8
The Experiments
14
Discussion
48
The
Pattern
of
Memory
Dysfunction
51
Theoretical Implications
59
ract ical Considerations
67
References
69
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ORSI
1 .
I t is
now known
tha t
in man
bi la te ra l lesions of
the
medial temporal
regions
of
the brain, involving both
hippocampi and
parahippocampal gyri , are
associated with
a
general ized,
severe, and
la s t ing
memory
disturbance
(Penfield
&
Milner, 9 5 8 ~
Scovil le &
Milner,
1957).
Milner
(1970)
describes t h i s disturbance:
"Patients
with
these lesions
show
no loss of
previously acquired knowledge or sk i l l ; nor
do they have any perceptual di f f icul ty . The
immediate reg is t ra t ion
of
new information
appears to
take
place normally, provided the
information
does not exceed
the
span
of
immediate memory.
Yet these pat ients seem
largely incapable
of adding
new information
to the long-term s tore ."
This
picture is supported
by evidence
from several experimental
s tudies ,
many of
which
are
based
on
observat ions
of a single,
important case.
Intensive
study
of
the pat ient H.M. who
underwent
bi la tera l
resect ion
of the
hippocampal zone for
the
re l i e f
of in trac table seizures (Scoville , 1968) has re -
vealed much about the nature of the anterograde amnesia which
follows damage to
t h i s area
of
the
brain.
Milner (1970)
has
shown
tha t
th i s
pat ient
is
capable of remembering subspan
verbal information for several minutes; however, as soon as
his at tent ion
is diverted
he forgets .
This finding is
consistent with
the
suggestion of Drachman and
Ommaya
(1964)
tha t amnesic pat ients can hold a
simple
memorandum for
long
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CORSI
2.
in te rva l s in t he absence o f d i s t r a c t i ng ac t i v i t y . Fur ther
s tudies
(Drachman
Arbi t , 1966)
have
demonstra ted
t ha t
pa t i en t s
with
b i l a t e r a l l e s ions o f the medial
temporal
reg ion
have
normal
immediate memory, but are unable to
l ea rn a se r i e s o f
d i g i t s
o r a
sequence o f l i gh t
pos i t ions
which exceed
t h e i r
immediate
memory span.
t seems
t ha t
as long
as
these
people
can verba l ly
rehea rse
the
mater ia l- to-be-remembered, t h e i r r e t e n t i o n i s
i n t ac t .
However, f
the
memoranda cannot be e a s i l y ver -
ba l ized , then the
oppor tuni ty
fo r
rehea rs ing
the mate r ia l
without
d i s t r a c t i on does not
benef i t
the
amnesic
sub jec t .
L.
H. Pr isko
(1963)
has used
t he
delayed
paired-comparison
method
o f Konorski (1959) to show p a t i e n t H.M. 's rapid
fo rge t t ing o f simple perceptua l informat ion which
could
not be verba l ly encoded. H.M. was unable to match c l i c ks ,
tones ,
shades
of r ed , l i g h t f l a shes , and
nonsense pa t t e rns
a f t e r
shor t
delays
up
to
60
seconds ,
whereas normal
subjects
showed no decrement in performance
over the
same i n t e rva l s .
Using a
delayed matching-to-sample
t echnique ,
Sidman, Stoddard
Mohr
(1968)
have confirmed Pr i sko s i n i t i a l f indings . They
observed a sharp d e t e r i o ra t i o n i n H.M. 's recogn i t ion
o f
non
verba l
mate r ia l
( e l l i p s e s )
over
r e t e n t ion in t e rva l s
o f
l e s s
than
30 seconds. At 32
second de lays , the
sample s t imulus
ceased
to exer t any con t ro l over H.M. 's
matching choice ,
while
fo r
normal sub jec t s accura te matching has
been
observed
fo r de lays
Of
40
seconds o r longer . In both o f t he se s tud ies ,
a
severe
r e t e n t i o n d e f i c i t
was
evident r egard les s o f
whether
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CORSI
3.
the
pa t ien t was
dis t rac ted dur ing the i n t r a t r i a l
i n t e rva l .
Most recen t ly
Milner Taylor
(1972) have
inves t iga ted
the
re ten t ion
o f
somesthe t ic informat ion fo r
pa t i en t
H.M. In
t h e i r
exper imental t a sk , the sub jec t was requi red to pa lpa te
an i r r e gu la r wire
shape
and then ,
a f t e r
varying delays , to
s e l e c t the
sample
shape
aga in ,
by touch, from a group o f
four s imi la r ones. H.M. was able to match the shapes a t
zero delay and
showed
normal intermanual
t r ans fe r ,
ye t h i s
recogni t ion dec l ined sharply
as soon
as a
de lay
was introduced,
and f e l l
to
chance beyond 30 seconds . Control pa t i en t s with
un i l a t e ra l co r t i ca l exc is ions showed e r ror le ss matching
with
i n t r a t r i a l in te rva l s of severa l minutes.
The exper imental s tud ies o f
globa l memory dysfunc t ion
a f t e r b i l a t e r a l l e s ions o f the hippocampal
zone, re in fo rce
o n e s c l in i ca l impressions o f pa t i en t s with
such l e s ions .
For these
people , the ongoing
events
o f
da i ly
l i f e
seem to
be
forgot ten
as
soon
as
the
focus
o f
a t t e n t ion
sh i f t s
to
o ther
occurrences and
so,
fo r the
most
par t ,
they
seem to
l i ve
from
moment
to
moment.
Yet,
t
has
recen t ly been shown
t ha t
the memory
l o ss in amnesic pa t ien t s
i s not as
complete
as
e i the r
t h e i r
behavior in everyday l i f e or in some formal
learn ing experiments
would
sugges t .
Moreover,
t
has
been
proposed (Milner , 1968) t ha t c e r t a in kinds of l ea rn ing
might even occur
a t
a normal r a t e . Milner , Corkin Teuber
(1968) have demonstrated t ha t
pa t ien t
H.M. was capable o f
some learn ing on s imple v i sua l and t a c tua l maze problems
with in tens ive
prac t ice . This pa t ien t was able to r e t a i n
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ORSI
4.
the solut ion of
a visual maze
up to one week a f te r
t ra in ing
to a s t r i c t cr i te r ion and when
tes ted
two years l a te r on the
same problem (Milner,
1970)
he
showed considerable
savings
(75
per
cent ,
even
though
he
had
forgotten
tha t
he
had
previously learned the
maze. Warrington Weiskrantz
(1968)
have
shown
tha t
amnesic
subjects can
learn to
recognize
fragmented drawings
of words and common objec ts , and
tha t
they re ta in th i s
form
of perceptual learning
for
several
weeks. This f inding has been confirmed by
Milner,
Corkin
Teuber (1968)
for the pat ient H.M., who learned to recognize
incomplete pictures
normally
and
demonstrated a
high
degree
of
re tent ion
a f te r
four months.
The most s tr ik ing example of sparing of learning
and
memory af t e r
bi la te ra l
hippocampal damage occurs with
respect
to motor sk i l l s .
Milner (1962)
was
the f i r s t
to
suggest tha t the acquisi t ion of motor habi ts might be
unaffected
by
hippocampal
lesions.
Following
t h i s
suggestion,
Corkin
(1968)
invest igated the performance of pat ient H.M. on
several
manual
tracking
and
manual coordination tasks . H.M.
showed learning
and
re tent ion of
motor
sk i l l s over several
days of te s t ing , although his
in i t i a l performance
was in fe r io r
to tha t of normal control subjects . This f inding,
in contrast
to
the
evidence
of
severe
def ic i t s
on
many
other learning tasks
for t h i s patient ,
is consonant
with
studies
in normal
subjects
which
have
established differences between
kines thet ic memory
and
memory
for words or visual locat ion (Posner, 1966; Posner
Konick,
1966;
Williams, Beaver,
Spence Rundell,
1969).
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CORSI
5.
To
d a t e
e f fo r t s to
reproduce
t he
hippocampal
amnesic
syndrome in
monkeys
have
proved
l a rge ly
unsuccessful .
t
has
been
demonstra ted
t ha t
analogous b i l a t e r a l l e s ions o f
the
medial temporal
region in monkeys do
not
produce
de f i c i t s
of the sever i ty and permanence repor t ed for
man
(Orbach,
Milner
Rasmussen, 1960; Drachman Ommaya, 1964; Cordeau
Mahut, 1964; Corre l l Scov i l l e 1965) .
The
most cons i s t en t
and reproduc ible e f f e c t
al though
not
invar iab le
(Dorff , 1964;
Waxler
Rosvold,
1970) , i s
a se lec t ive impairment on spa t i a l
de layed-a l t e rna t ion
but not
on delayed-response t a sks
(Mahut
Cordeau, 1963;
Corre l l Scov i l l e
1967; Mahut, 1971) .
In
add i t ion a genera l defec t in v i sua l d isc r imina t ion l ea rn ing
has
been found to be assoc ia ted
with b i l a t e r a l
inferotemporal
l e s ions in the monkey (Mishkin, 1954; Mishkin
Pribram, 1954) .
Further
experiments ( Iwai Mishkin, 1968; Iwai Mishkin, 1969)
have
revealed t ha t
the impairment produced by l a rge i n fe ro
temporal
l e s ions
involves
a t l ea s t two d i s t inc t
components;
with pos te r io r
damage to t h i s
a r ea
a l o ss
in
v i sua l
pa t t e rn
percept ion has been observed, whereas more a n te r io r
l e s ions
have resu l t ed in
defec t s
o f
v i sua l learn ing and
re ten t ion .
Recently ,
Iversen Weiskrantz
(1970)
have shown t ha t hippo
camp a l l e s io n s
aggravate
the
d e f i c i t in
pa t t e rn and ob jec t
d i sc r imina t ion l ea rn ing a f t e r b i l a t e r a l
inferotemporal
damage.
These authors have proposed i n l i ne
with
Iwai Mishkin (1969)
t ha t in
the
monkey, the
pos te r io r
in fero tempora l cor tex
i s
concerned with
perceptua l
ana lys i s whereas the
a n te r io r
temporal cor tex
including
the medial s t ruc tu r e s mediates
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CORSI
6.
the
encoding o f
new
informat ion;
and
they fur the r
sugges t
t ha t fo r
man these mechanisms have evolved to process
ve rba l
in add i t ion to
non-verbal
events . S t i l l t i s evident t ha t
a l though
some
learn ing defects
have
been
found
fo r
monkeys,
they have not
been
of the
magnitude
or kind observed
in
pa t i en t s
with
b i l a t e r a l
hippocampal l e s i o n s and these f ind ings
sugges t
an evolut ionary d i scon t inu i ty between monkey and man in the
func t ion o f the medial
temporal
s t ruc tu r e s .
In con t ras t t o the
globa l
memory dis turbance
produced
in
man
by
b i l a t e r a l
l e s ions
in
the
hippocampal zone, t he e f fec t s
o f
un i l a t e ra l
l e s ions o f the temporal lobe
are f a r l e s s
severe
and s pe c i f i c a l l y
r e l a t e d
to the
na ture
of the informat ion presen
to
the
pa t i e n t .
Although
r a r e ins tances o f pe r s i s t e n t
amnesia
have been repor t ed
a f t e r
un i l a t e ra l temporal lobectomy, these
a re usua l ly
seen only
i n pa t i en t s with e lec t rograph ic
or
rad io log ica l
evidence o f add i t iona l
damage
to the
opposi te
temporal lobe (Milner , 1966) .
In genera l
people
with
l e f t
temporal - lobe
l e s ions
in
the dominant
hemisphere fo r
speech
t yp i c a l ly show impairment
on
verba l learn ing and verba l
memory tasks (Meyer Yates , 1955; Milner , 1958) . This
d e f i c i t i s
observed
i r r e spec t ive
o f whether the ve rba l
mater ia l to
be
remembered i s heard
or read
(Milner ,
1967;
Blakemore Falconer , 1967) . Fur ther t i s not dependent
on the sp e c i f i c method by
which verba l
r e t e n t i o n i s
assessed
(Milner ,
1958;
Milner Kimura,
1964;
Milner Teuber , 1968) .
With
corresponding
l e s ions
o f the r i g h t nondominant hemisphere,
verbal
memory remains normal;
however ,
the r e t e n t ion o f "non
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CORSI
7.
verba l informat ion , such
as
complex v i sua l or aud i to ry
pa t te rns ,
i s
se lec t ive ly
impaired (Kimura,
1963; Prisko,
1963;
Milner ,
1968;
Shankweiler,
1966; Warrington James,
1967) .
People
with
r i gh t
temporal lobectomies
a l so
show
a
l ea rn ing
d e f i c i t
fo r
both
v i sua l and propr iocep t ive
maze
problems (Corkin ,
1965;
Milner ,
1965) . The performance
o f
pa t i en t s with
l e f t
temporal lobectomies i s
i n t ac t fo r a l l o f
these
non-verbal
t a sks .
Within
the l a rge
group o f pa t ien t s
a t
the Montreal
Neurological I n s t i t u t e
who have undergone un i l a t e ra l
temporal
lobectomy fo r the r e l i e f o f focal ep i lepsy , t he re i s a wide
var i a t ion in the sever i ty o f
these
mater i a l - spec i f i c
re ten t ion
d e f i c i t s . Since the su rg ica l removals usual ly
involve
the
hippocampus and parahippocampal gyrus as
wel l
as the l a t e r a l
neocortex, it i s
important
to the
understanding o f
ce rebra l
organizat ion o f func t ion and
b ~ i t i d l
on
c l i n i c a l grounds
to
f ind
out
whether
the
sever i ty o f
the
memory
dis turbance
i s
r e l a t e d to the
degree o f
damage to
these medial
s t ruc tures .
Milner (1967) has
t e n t a t i ve ly suggested t ha t l e f t hippo
campectomy may increase
the
verba l learn ing
impairment seen
a f t e r
removal
o f the l e f t
temporal
lobe .
Furthermore, it
has
been shown t ha t
fo l lowing
r i gh t temporal lobectomy, a
d e f i c i t in maze l ea rn ing occurs , i and only i the bulk o f
t he hippocampus i s
removed on the
r i gh t s ide (Milner , 1965;
Corkin, 1965) ,
and
t he re i s some i nd ica t ion t ha t
the same
i s
t r ue
fo r the
impairment in
r ecogn i t ion
o f unfami l i a r
photographed
faces
(Milner , 1968) .
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CORSI
8.
The Present
Inves t iga t ion
The
s tud ies
to be repor ted here were s pe c i f i c a l l y
designed to
br ing
out the ro le o f
un i l a t e ra l
hippocampal
l e s ions in
mater i a l - spec i f i c
memory dis turbances .
The
tasks
used
to assess mnemonic
func t ion
were t e s t s o f shor t - t e rm
r e t e n t ion and l ea rn ing with i n t e rpo la t ed ac t i v i t y . In
add i t ion
to
groups of
normal sub jec t s and pa t i en t s with
un i l a t e ra l
t empora l - lobe exc i s ions the
well-known
pa t i en t
H.M.,
with
b i l a t e r a l
hippocampal damage
was a l so
examined.
This
man's performance provides a reference
from
which
to
eva lua te the extent o f the
memory
dis turbances fol lowing
un i l a t e ra l
t empora l - lobe
surgery .
'8u'bjects
The
people
who
were s tudied
were
pa t i en t s a t the Montreal
Neurological
I n s t i t u t e . All o f
these pa t ien t s underwent un i
l a t e r a l temporal
lobectomy
fo r the r e l i e f of foca l ce rebra l
se i zu res .
The
cause
o f
the se izures
in most
of these
people
was
foca l ce rebra l
atrophy
dat ing from b i r th
or
ear ly l i f e
a l though a few
cases of adu l t
head i n ju ry were
a l so inc luded.
Pat i en t s
with evidence
of d i f fuse
cerebra l
damage, or with
epi lepsy of unknown or ig in were
excluded, as
were cases
o f
i n t r ac ran i a l tumor.
Moreover, Wechsler In te l l igence and memory
quot ients were known fo r a l l
pa t i en t s
and
t
was poss ib le to
e l imina te
those
with
an
I .Q.
r a t i ng
below
70. Altoge ther 9
pa t ien t s who underwent l e f t
temporal lobectomies and
9
pa t i en t s
wi t h
r i gh t
t empora l - lobe
removals were
s tud ied .
These
two group
inc luded
only
people with speech rep resen ta t ion in t he l e f t
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CORSI
9.
hemisphere as demonstra ted by c o r t i c a l s t imula t ion and, in
some cases ,
by
the Wada 1949) technique of i n t r a c a ro t id
in jec t ion
o f sodium
y t a l ) . The major i ty of
pa t i en t s
were
t e s t ed in
long- term
1-10
years)
fo l low-up , a l though
19
pa t i en t s in the
r i gh t
temporal - lobe
group
and 15 pa t i en t s in
the
l e f t temporal - lobe group were t e s ted t h ree
weeks
a f t e r
operat ion . Most of the
pa t ien t s were
on small doses o f
barb i tura te s , and t he re were no systematic group
d i f fe rences
with r espec t to the na ture or amount
o f
t h i s ant i -convulsant
medicat ion.
In
order
to i nves t iga te the
spec ia l ro l e
o f
the
medial
temporal - lobe
s t ruc tu res in
mate r i a l - spec i f i c
r e t e n t i o n
d i so rde rs ,
the
r i gh t and l e f t temporal - lobe groups were each
divided i n to four
sub-groups
depending on how
much
o f the
medial temporal
reg ion
was
removed. A c l a s s i f i c a t i o n system
suggested by Dr.
Theodore
Rasmussen was
u t i l i zed in
making
t h i s
subdivis ion ,
and
the
hippocampus
served
as the
bra in
mark
fo r
de l inea t ing
the extent o f medial temporal - lobe
excis ion . The
surgeon s
measurement o f
excised t i s sue a t
the t ime o f opera t ion
was
used in
ass igning a pa t ien t
to
a
sp e c i f i c sub-group.
The four
l e f t
temporal sub-groups are i l l u s t r a t e d by
rep resen ta t ive
cases
in
Figure
1 .
Figure
pre sen t s
the
analogous
informat ion
fo r the
r i gh t
temporal group.
The
removals in
every
case
inc luded the
uncus
and
amygdaloid
nucleus,
but the extent of
removal
of the
hippocampal
complex
hippocampus, parahippocampal gyrus , and fus i form gyrus) va r i ed
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Figure,
1
.. i-,
REPRESENTATIVE LEFT TEMPORAL LOBECTOMI
EXTENT O MESIAL REMOVAL
GROUP
1 GROUP 2
GROUP 3
Pes Hippocampi nd
Hippocampus Spared
Pes Hippocampi Excised
approximately cm
of Body Excised
Case T H Case R S
Case J W
Note.;.. Brain maps
based on , the surgeon s drawings a t
of operation, showing representat ive l e f t temporal l
n four groups of pa t ien ts
classed
according to the
hippocampal destruct ion
L a ~ 1 ~
s \ g _ f c 3 . c e ~ ~ Q . Q y e ;
me_d
below. S t r p p ~ l e d a r e a Indicates extent of cor t ica l
e
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F i ~ u r e
2
~ r : ~ R E S f : N T
A1 1Vr: n D ( ? : ~ n ' -
T r ; 1 ' v ~ P O n . A l l O r n ~ C T O r l l l ~
X T ~ N T OF w ' H : 5 ~ A L ~ r . : l ' . ~ O V A .
GROUP 1
Hippocampus Spared
i
r
(
ea.-
M.A.
I
G n o u ~ 2
Pes Hippocampi Excised
.....--
..........
.ain maps based on
G l O U ~ 3
Pes
Hippocampi and
approximately
1 cm.
of
Body E ) ~ c i s e d
CaiU S.M.
the surgeon ' s
drar,.]ings
a
of op
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CORSI 12.
cons iderab ly from pat ien t to
pa t i en t .
As
ind ica ted by the
f i gu re s , Group
I
for
each
ser ies cons i s t s of
pat ien t s
in
whom
the medial
aspect of
the temporal
lobe
was
en t i r e ly
spared.
In
Group II
the
pes hippocampi was
removed, but
the body o f
the
hippocampus was l e f t i n t ac t . Group T I l i s
composed of pat ien t s
with
medial removals t ha t inc lude
the
pes hippocampi and one addi t i ona l cent imet re
o f the body of
the
hippocampus.
The
pat ien t s in Group V underwent r ad i ca l
removal of
the
hippocampal zone. The medial excis ion in
these cases was
ca r r i ed
back l a t e r a l to
the
bra in stem.
The exten t of l a t e r a l c o r t i c a l
removal
(measured a t the
Sylvian f i s s u r e and the base of
the temporal
lobe re spec t ive ly)
for the d i f f e ren t l e s ion groups i s
presented
in Table 1 .
Across
the
l e f t temporal - lobe sub-groups no s ign i f i can t va r i a t i on i n
terms of
the
l a t e r a l exten t o f
removal
a t the Sylvian Fissu re
(F = 1.39,
P
>.25) or a t
the
base of t he
temporal
lobe
(F
=
0.26, P
>.25)
was
observed.
Simi lar ly ,
no s ign i f i can t
va r i a t i on was found for t he
r igh t
temporal sub-groups, for
removal
along the Sylv ian f i s s u r e
(F = 1.52, P >.25) o r a o n g
the base of the temporal lobe (F
=
0.69,
P >.25) .
Age and
i n t e l l i gence - t e s t
da ta for the
var ious
pa t i en t
sub-groups a re
given in
Table 1 . As
i nd ica t ed , 2 normal
cont ro l
sub jec t s
s tudent nurses and
t echn ic ians )
were also
t e s ted , and
t he re
was no s ign i f i can t va r i a t i on for
the
r igh t
and l e f t
temporal groups
and the
cont ro l group
with r e spec t
to age (F = 2 4 ~ P >.25) .
In
addi t i on ,
the
temporal - lobe
groups did not
d i f f e r
s ign i f i can t ly
with reference
to Wechsler
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CORSI
13
r ~ a b 1 e 1
Age, Lateral Extent of Removal, and Follow-up I.Q. of
DiHerent Lesion Group
Mean
Lateral
Removal
em)
Mean
Mean
Group
N
Sylvian
Bale of
Age
Fissure Temporal Lobe
Wechller
I.Q.
ormal Control 20
28 1
-
-
ot
Tested
Left Tern poral
39
30.9
5.2 5.9
104 1
Left Temporal
Sub-Groups I
9
29.6
5.6
5.9
1037
10 28.3
5 1
5.9 106.7
30.8 5.4
6 1
104.0
IV
9
35.2 4.7
5.7
1017
Right Temporal
39 26.5
5.7 6.6
105.5
Right Temporal
Sub-Groups I
7
21 3
6.2
7.3
102.7
14
30 1
5.6
6.6
107 1
7
22 1
6.3 6 9
106.4
IV
26 1
5.5
6.2
104.9
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ORSI
14.
Bellevue
In te l l igence t e s t scores (F = 0.11,
P >.25). I t
should
be noted
tha t because
the research reported here was
conceived progressively, there is
some
minor variat ion
in
the
composition
of
the
different
pat ient
groups
for the
re tent ion
s tudies
tha t
follow.
In
a l l
cases
th i s
var ia t ion
is
ins ignif icant and
Table
1 thus serves as
an
overa l l summary
of the indicated variables across these
s tudies .
In
addition
to
the
uni la te ra l
cases,
the
'patient
H.M.
(Scoville ,
1968) who underwent a radical
bi la te ra l medial
temporal-lobe
resect ion for the
r e l i e f of generalized
seizures
was
also studied.
In
H.M.,
the surgical
removal
was
said
to
extend
poster ior ly
along
the
medial
aspect
of
the
temporal lobes
for a
distance of
8
centimetre,S
from the
temporal
t ips , thus destroying bi l a t e ra l ly the
anter ior
two-thirds of
the
hippocampi and
parahippocampal
gyri , as well
as the
unci
and amygdalae, but
sparing the l a te ra l neocortex.
At
the
t ime
of
t es t ing,
15
years
a f te r
operat ion,
th i s
man was 42
years
old with
a
Wechsler I.Q. of 118. In order to
highlight
the
special nature of t h i s pa t i en t s memory distur.bance, his
performance wil l
be
considered separate ly
from the
group data.
,
The
Expe r im:e nt s
Altogether ,
four
short- term
re tent ion
s tudies
were carr ied
out.
Two
of these
tasks required
the
r eca l l
of
verbal
in
formation and the
other
two
required
the
reca l l
of non-verbal
information.
Verbal S'ttidies
Re'ca ' l lofconsonant t r igrams. This verbal
memory task,
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CORSI 15.
which i s
a
s impl i f i ed
vers ion
o f the
Peterson
and Peterson
(1959)
technique,
requ i red the r eca l l of ind iv idua l ly
presented ,
consonant
t r igrams. The t r igrams were
se lec ted
to
be
o f
equa l ,
low
assoc ia t ion-va lue
(Witmer,
1935) .
n
any given t r i a l , a t r i g ram
followed by
a 3-d ig i t number e .g .
DFX357 )
was
read aloud
to the
pa t ien t a t
the
r a t e
o f one
l e t t e r or
number)
per
second.
His t a sk
was
to
r epea t
t he
number immediately
a f t e r
hear ing
t
and then to
count
backwards
from t as
quickly
as
poss ib l e
un t i l
he was
s igna l led by the
onset of a red l i g h t to
s top
count ing and r e c a l l the consonant
t r i g ram t ha t
preceded the
number
e .g .
DFX ). The pa t ien t
was
given 15
seconds in
which to r e c a l l
the
l e t t e r s and
then
a
new t r i a l began.
In
t h i s
des ign,
the counting
served
as
a
device to
keep
the sub jec t
from
rehears ing the
3
consonant
l e t t e r s .
Pi l o t
s tud ies
had
demonstra ted
t ha t
the or ig ina l
d i s t r ac t o r
t a sk employed by
Peterson
and
Peterson (1959)
in
t he i r
study
o f
normal
col lege s tudents
(counting
backwards
by
th ree
in
t ime to
a
metronome) was too
s t r e s s f u l
fo r t he p re sen t
pa t i en t popula t ion , and t he re fo re
the
pa t ien t s
were
simply
reques ted to count backwards as rap id ly
as poss ib le .
They
were a l so t o ld
t ha t t he
counting was
j u s t
as important as
remembering
the l e t t e r s .
There
were
6 condi t ions
ln
the
exper iment ,
the
var iab le
being the length
o f
the
r e t e n t ion i n t e rva l ,
namely, 3, 6, 9,
12, 15 o r
18 seconds. Altoge ther 4 t r i a l s were conducted
fo r
each
sub jec t , with 4 t r i a l s occurr ing
a t
each
o f
the 6
re t en t ion
i n t e rva l s .
The score
was
the t o t a l number of l e t t e r s
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ORSI
16.
correc t ly reca l led for the 24
t r i a l s .
With
normal
control subjects the decline in correct
reca l l for th i s task becomes quite marked as the
re tent ion
interval
gets
longer
(Figure
3).
Analysis
of
variance
on
reca l l scores
for the combined
normal-control,
lef t- temporal ,
and r ight- temporal groups
yielded an
F-rat io of 48.91 (p
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17
CORSI
100
0
c
90
0
c:
0
0
80
0
u
70
II
at:
u
II
60
0
u
II
u
50
II
Q.
c
40
0
II
E
Figure 3
Verbal
Recall as a unction of Retention
Interval
in Normal
Subiects
N=20)
~
~
.
.
3 ~ ~ ~ ~ ~ ~ ~
3 6 9 2 15
18
Retention Interval {Seconds}
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CORSI
18 .
Figure 4
Verbal
Memory efect
after
Left
Temporal Lobectomy
. .
..
.
. . . . .
.
. .
. . ... . . . .
. . . .
.
..
.
.
.
.
. .
.
. .
. . . .
. .
.
.
.
. . . .
.
. . . . . . ..
.
.
.
. .
Normal
Subjects
. .
.
.
. . . .
.
. .
. .
.
.
. .
.. . . .. . . . . . . . .
. . . . . .
.. ... . .
. . . .
. . . . .
.
.
. . . .
. . .
.
.
. . . .
.
.
.
.
.
.
. . . . .
. .
. . .
..
. .
. . ....
N=20)
. .
.
. . . ..
.
. .
. .
.
. .
. .
. . . . .
.
. . . .
.
.
..
..
.
... .
.
. . .. . . . . . . ..
.
. . . .
.
..
Right
Temporal
N=30)
Left Temporal
N=38)
o
10
20
30
4
50
60 70
80 90 1
Peterson Task:
Mean
per
cent Correct Responses
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19 .
CORSI
Table 2
Recall
of
Consonant Trigrams
for
DiHerent Lesion Groups
Group
N
Mean
Corred
Recall
Normal Control
20
77.8
Right Temporal
30
78 1
Left
Temporal
38
58.3
Sub Groups
I
9
72.5
10
60.4
III
10 52.4
V
9
477
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CORSI
20.
Figure
5
ba
l Recall as a unction
of Retention
Interval
er
1
:! 9
c
o
c
o
80
o
U
;
70
o
u
CI)
a
-
u
60
CI)
o
U
50
-
CI)
u
i 40
Q.
c
o
CI) 30
~
20
Normal
Controls
Right
Temporals
lell Temporals
Group I
.
. ~ '
~ ~
, , ____
roup
IV ~ o 0
_____
- ~ ~ o
. ~ = = : . ~
I
9
12
15
o
-
J ~ ~ ~ ~ ~ ~ ; : : : : . : . ~ ~ I ; ~
18
3
I
6
.
I {Seconds}
Retention
Interva
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21.
Figure
6
Verbal
Memory efect after Left
Temporal
Lobectomy
as
related
to
Mesial Extent
of xcision
. . . . . . . . . . . . .. . .
. .
.
. . . . . . . . . . . . . . . . . .
.
. . . . . . . . . . . . . . . . . . . .
Right Temporal
.
. . .
. . . . .
.
. . .
. .
. . . . . .
. .
.
.
. . .
.
. . . . . . . .
.
. .
.
N=30
Left
T
em
pora I spa r I ng
hippocampus N=9
Left
Temporal incl. pes
hippoc. N=10
o
(!)
Temporal incl. pes
+ 1 cm body hippoc. N=lO
Left Temporal with maximal
hippoc. removal N=9
o
1 20 30 40 50 60
70
80 90
100
Peterson Task: Mean per cent
Correct Responses
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CORSI
22.
subdivided in to 4
groups
depending on
the
extent of
medial
temporal removal,
using
the same c r i t e r i a as for l e f t
temporal
c lass i f ica t ion
However, no
s ignif icant var ia t ion
was
found
across
the
four
r ight- temporal
sub-groups
(F
=
0.83,
p >.50) on th i s
verbal
task.
The
severi ty
of
the verbal memory
def ic i t
in
th i s
experiment was found
to be
direc t ly
re la ted
to the
extent
of the encroachment upon
the
hippocampal
zone in the
dominant
hemisphere for speech. For pat ients
sustaining extensive
surgical
removals of
the
medial
temporal-lobe s t ruc tures in
the l e f t hemisphere, there i s an impairment in the ab i l i t y
to
hold
verbal inputs for even
very short
in tervals
when the
opportunities
for rehearsal are r es t r i c t ed From
th i s
study,
there
appear to be
no
sharp discont inui t ies between the
per
formance
of people with large
medial
temporal-lobe
excis ions
and
tha t
of normal control subjects
(see
Figure 5). Even
though
the
verbal
reca l l
of
l e f t
temporal
pat ients
in
Groups I I I
and
IV
1 S quite impoverished
re la t ive
to other groups, the
retention curves obtained for the various groups run roughly
para l le l
to
each other .
Hebb
, s r ecu r r i ng dig its
task. This
next experiment was
a further
attempt to
understand the nature of the
verbal
memory
impairment which
resu l ts a f te r lesions of the hippo
campal
zone in
the dominant hemisphere for speech. The
design
of th i s task follows
from
an experiment
or ig ina l ly
conducted
by
Hebb (1961). In
the present
study, the immediate memory
span
for dig i ts was
f i r s t ascertained
for a l l subjects by
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CORSI
23.
the
method o f
Wechsler 1944) . The
sub jec t
was next
presented
with 4 sequences o f d ig i t s ,
one
sequence
a t a t ime. Each
sequence was
one d i g i t in excess of the pa t i en t ' s
immediate
memory
span.
So,
fo r
example,
i
a
person
was
able
to
r eca l l
7 d i g i t s in
co r rec t
order immediately
a f t e r
hear ing
them,
then
he was presented
with 24
sequences
o f 8
d i g i t s
each.
The
sequences
were
read
aloud a t
the r a t e
o f one d ig i t
per
second,
with a IS-second
i n t e rva l between
sequences . The sub jec t was
simply i n s t ruc ted
to repeat
each sequence immediately, in
the
exact order
o f
presenta t ion . For t h i s t a sk , t he re was one
spec ia l
fea ture
about
which
the
pa t ien t
was not informed: on
every
t h i rd
t r i a l
(3rd , 6 th ,
9th
24th)
the
same se r ie s
of d i g i t s was
repeated ,
whereas
the o ther
in te rvening sequences
occurred
only once.
Two performance scores
were
obta ined fo r
t h i s
t a sk .
The
f i r s t
score was the number
of r ecur r ing
sequence
which were reca l led in cor rec t order 7 maximum) and the second
was t he
number
o f non-recurr ing
sequences
cor rec t ly reca l l ed
17 maximum). In scor ing , the
f i r s t presen ta t ion o f the
repeated sequence was t r e a t e d
as
a non-recurr ing sequence.
With normal sub jec t s , Hebb 1961) has shown
and
Melton
1963)
has
confirmed t ha t
r eca l l
of
the r ecur r ing
sequences
improves progress ively over r epe t i t i ons , whereas no s ign i f i c a n t
cumulat ive
improvement
occurs
fo r the
non-repeated
sequences .
In 1961,
t h i s f inding convinced Hebb
t ha t
some s t ruc tu r a l
t r ace may be
es tab l i shed very
ea r ly in
the memory
process .
I t
i s
o f i n t e re s t to analyse the
performance
of pa t i en t s
with
dominant , l e f t
temporal lobectomies
on t h i s t a sk because
it
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CORSI
24.
provides
a nice
method
for fol lowing
the
course o f verbal
learn ing and, presumably, the course
of
consol ida t ion of
memory t r aces over a shor t ser ies of
t r i a l s .
To
da te ,
pat ien t s
who
have
undergone
r i g h t
temporal
lobectomy, 9 pat ien t s
with l e f t
temporal - lobe removals
and
17 normal cont ro l
sub jec t s
have been examined on t h i s t a sk .
These groups
are
comparable
with
regard
to
age, i n t e l l i gence
and immediate memory span for d ig i t s F = 1.06 ,
P >.25) .
The
mean
d ig i t
span fo r
t he th ree
groups was
as
fol lows: normal
cont rol sub jec t s 6.7 ;
r igh t
temporal
pat ien t s 6.5;
l e f t
temporal
pat ien t s
6.3 .
In addi t ion, no
s ign i f i can t
var ia t ion
was observed for t h i s var i ab le across the
four
l e f t temporal
sub-groups F = 0.01,
P
>.50) .
Analysis of
var iance for
the combined
l e f t temporal , r igh t
temporal , and normal
groups yie lded
an F- r a t i o of 19.93 p
-
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250
Figure 7
Hebb
Digits Task:
Mean
Per Cent
Corred
Digit Sequences
for
Total Temporal lobe Groups
1
en
C1
Recurrent Sequences
Non recurrent
Sequences
u
C
C1
::;
8
t
C1
.
.
'
..
-
1
6
u
o
u
. .
..
. .
-
.
.
.
0
C1
.
C1
.
. .
.
.
.. .
.
. .
2
.
C1
.
.
...
.
.
.
.
o
Normal
Right Left
Normal
Right
Left
Control
Temporal
Control Temporal
(N=17) N=33)
N=39)
N=17)
N=33)
N=39)
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26.
Table 3
Hebb
Digits Task:
Mean Per
Cent
Corred
Digit
Sequences
for Left Temporal Subgroups
Mean Per
Cent Corred
Sequence.
Group
N
Recurrent
Sequence.
Non-Recurrent
Sequence.
Right Temporal
33
77.4 23.4
Left Temporal
9
73.0
22.9
Left Temporal
61 0 19 2
Left Temporal
10
32.9
20.6
Left Temporal V
9
28.6
15 8
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27.
Figure
8
ebb Digit Task Mean Per Cent Corred Digit Sequence
as a Fundion of Ordinal Presentation of Recurrent Item
100
D
o 80
U
en
D
'
Normal Control 4
;
;:)
60
Left Temporal
C
D
CI
Group
I
A---A
C
40
Group
II
0 0
D
U
D
Ill. 20
Group III 0--
Group
IV
c
c
D
12 15
8
21
24
Item Number for Recurrent Sequence
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28.
l e f t
temporal
sub-groups for the
recurring
sequence
scores
revealed
s ignif icant var ia t ion across these groups F =
11.90,
P .2S) . Those pat ients
with
the hippocampus
spared
(Group I) correct ly recal led the
recurring
digi t sequence more frequently than
pat ients in
Group
I I t = 1.81, P .2S)
or
normal
control subjects t = 0.82
P >.2S). However, pat ients with the
pes
hippocampi excised in
the l e f t hemisphere (Group I I )
did
show an impairment
for reca l l
of
the recurrent
sequence
re la t ive
to the r igh t
temporal
pat ient
t
=
2.91,
P
.SO>
From
the
analysis of resu l ts
for
the Hebb digi ts- taSk t
i s apparent
tha t the magnitude of
verbal
learning impairment
i s
proport ional to
the extent of
medial temporal-lobe excision
in the
dominant
hemisphere for speech.
For pat ients
with
large
medial
removals of the l e f t
temporal- lobe,
the consol idat io
of
verbal impressions over time
seems
part icularly susceptible to
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disrupt ion, although immediate memory
as
sampled by span tasks
remains re la t ive ly unaffected. Thus,
whether
one
chooses to
study the
course of forget t ing (as in the Peterson task)
or
the course of
verbal
learning in these
pat ien ts t i s
evident
tha t the hippocampal zone in the l e f t
hemisphere
i s
spec i f ica l ly
involved
in the verbal consolidation process.
Studies of
Non-Verbal Retention
and Learning
In
the two
experiments
described thus
f a r the severi ty
of verbal memory impairment was found
to vary
direc t ly with
the extent of encroachment
upon
the hippocampal region in the
dominant hemisphere
for
language. From
what
i s known
of hemi
spheric specia l izat ion of function, t i s
reasonable
to look
for a
corresponding
re la t ionship
between
the
reca l l of non
verbal information and the in tegr i ty of the medial portion of
the r ight temporal lobe. For the
two
previous
s tudies
pat ients
with r igh t
temporal-lobe
excisions showed
normal
r eca l l of the
verbal
information presented
to
them,
regardless
of
whether
or not
the
hippocampus
was spared.
However, pat ients with
r igh t temporal-lobe removals do show a memory def i c i t in the
performance
of cer ta in non-verbal tasks (Kimura, 1963; Milner,
1968;
Shankwei1er,
1966).
The
extent to
which
th i s memory
impairment
can
be re la ted to
surgical
encroachment upon the
hippocampal
zone
in
the r ight hemisphere
i s
the focal problem
in the
following
two studies of learning and
re tent ion
for
non-verbal materia l .
Bl6ck Tapping Task. This task i s
iden t ica l
in design to
the Hebb
digi t s
task but
the items
are spa t ia l not
numerical.
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The t e s t mater ia l
(see
Figure
9)
consis ted of 9 black blocks
(1-1/4 cubes)
which
were
impart ia l ly arranged on a
black
board
(9 x 11 ) .
The
examiner
tapped
the blocks with a 6
wooden
s t ick
in a par t icu la r sequence and, immediately
the reaf te r , the pat ient was required to tap out exactly
the
same pat tern .
The pa t i en t s immediate
spa t ia l
span ( i . e .
the
maximum number of blocks he was
able
to tap in correct
order) was f i r s t
ascertained
and then 24 block sequences
which were
each one block
in
excess of the pa t i en t s immediate
span
were presented.
Each block
was
tapped only once in
any
part icular sequence with a 15 in te rva l between sequences.
As with
the
Hebb
digi t s - task ,
every
3rd
block sequence (3rd,
6th, 9th 24th) was repeated, whereas
the
intervening
sequences
occurred only
once.
The blocks were
numbered
on
the
examiner 's
s ide of the board for
ease
in recording the
pa t i en t s performance. However, from his posi t ion, the pat ient
was
unable
to
see
the
numbered
block
faces.
Two
scores
were
obtained:
the f i r s t was the number of recurring block sequences
which
were tapped
in correct order (7 maximum), and
the
second
was the number
of
non-recurring sequences correct ly
tapped
(17 maximum). In scoring,
the f i r s t presentation
of the
repeated sequence was considered as a non-recurring
sequence.
Thus far , 24 pat ients
with
l e f t
temporal-lobe
removals,
36 pat ients
with r igh t temporal-lobe
removals, and 16
normal
control
subjects have
been t es ted .
The mean immediate span
for block
tapping
for
these
groups was as follows:
normal
control
4.9;
l e f t temporals
4.9;
r igh t temporals 4.8 . No
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31.
>
.,
c
E
a
>.50). Furthermore,
no s ignif icant variat ion
was
observed for block
span
across
the four r igh t temporal
sub-groups (F
=
1.42,
P >.25).
Analysis of variance for the combined
r ight
temporal,
l e f t temporal,
and
normal groups yielded an
F-rat io of
15.93
(p
-
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33.
Figure
10
Block Tapping Task: Mean
Per
Cent
Corred
Block Sequences
for Total Temporal lobe Groups
Recurrent Sequences
Non Recurrent Sequences
en
CI)
u
C
83.9
80
D
CI)
en
e
60
53.9
o
u
-
u
CI)
D
C
c
CI)
E
40
20
.
. .
.
.
.
..
.
.
..
..
.
.
.
.
..
.
..
.
.
..
.
.
..
.
.
~ M ~ ~ ~ ~ ~ M ~ ~ _
26.9
21.2
..
.
.
.
..
.
.
..
.
Normal Left Right Normal
Left
Right
Control Temporal Temporal
Control Temporal Temporal
(N=16) (N=24) (N=35)
(N=16)
(N=24) (N=35)
-
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Table
4
Block
Tapping
Task: Mean
Per
Cent Corred Block
Sequences for Right Temporal Subgroups
Group
N
Mean Per Cent Corred
Sequences
Recurrent Sequences
Non Recurrent Sequences
Left Temporal
24 83 9 26 9
Right Temporal
7 77.6
227
Right Temporal
12 69.0
23.5
Right Temporal
7
42 9
227
Right Temporal V
1
28.6 15.9
-
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35.
Figure
11
Block Tapping
Task:
Mean
Percent Correct lock Sequences
as a Function of
Ordinal
Presentation of Recurrent
Item
100
-
u
Q)
"
0
U
en
Q)
u
c
80
, / - ~ . V
Normal Cont ro l . e
Right Temporal
Q)
:::)
e-
60
Group
I
.--&
Q)
-
Group
II
0 0
c
Q)
u
"
Q)
c
c
c
Q)
40
20
/
0 / ~
~ .
--/
Group m
0 0
Group
rsz
. .
3
6 9 12
lS
18
21
24
Item
Number for
Recurrent Sequence
-
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36.
con t ro l s
fo r r eca l l of the recur ren t sequence (Group I vs
Cont ro l s ,
t
= 0.31,
P
>.50; Group I I
vs Cont ro l s , t
= 1 .37 ,
P
>.25) .
In
con t r a s t , the pat ien t s
with
more extens ive
medial removals in Group
I I I
did show an
impairment
when
compared with
normal cont rol
sub jec t s
t = 4.71 , P .50) .
The r e s u l t s
of the
block- tapping analys i s
a re analogous
to
the f ind ings
fo r
the
Hebb
d ig i t s
t a s k . The
r i gh t
temporal
pat ien t s show a de f i c i t
in
non-verbal , s p a t i a l
learn ing
and
t h i s de f i c i t var i e s
d i rec t ly
with the ex ten t o f medial temporal
removal. Whereas the l e f t temporal pa t i en t s have d i f f i cu l t y
in
the conso l ida t ion
of verbal impressions
over
t ime,
the
r igh t
temporal
pat ien t s show
a
consol ida t ion
impairment
for
non-verbal mate r i a l . This
impairment
i s
apparent
even
though
immedia.te,
non-verbal ,
memory span, as
measured
by the new
block- tapping technique,
i s normal r e l a t i ve t o cont ro l sub jec t s .
RecaT lo f Visua l in fo rma t ion (Posner t ask).
The
f i na l study
in
t h i s
s e r i e s
o f experiments
was designed to analyse
fur the r
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37.
the
non-verbal
memory disturbance tha t resul t s
from
medial
temporal
excis ion in the r igh t
hemisphere.
The experimental
task
was a modified
form
of a simple t e s t which Posner
(1966)
has ut i l ized in his s tudies of
the
short- term re tent ion of
visual information. The
material
to be
reca l led
consisted
of a
1/4
inch-diameter c i rc l e located
a t
one of 4
posi t ions
along an 8-inch l ine . The
4
posi t ions , in mill imetres from
the l e f t end of the l ine are
indicated
in Figure
12. This
f igure
also serves
as
a summary of the experimental
design.
The
randomized t e s t
mater ia l was
presented
to the subject
on
a 3 x
23" panel . As i l lus t ra ted
in Figure 13, an
inspection
l ine with a small c i rc l e on t
appeared
in
the
presenta t ion
window to
the subjec t s l e f t
and was reca l led
by
him on a
t e s t l ine which appeared
in
the
reca l l
window
to
the r ight .
The information to
be
remembered
( i .e . - - -D---)
was exposed
in the presenta t ion window
for
5 seconds
during
which the
subject
marked
the
l ine a t
the center of
the
ci rc le
with
a
pencil stroke. The inspection stimulus was then
covered
and
af ter a short re tent ion in terval the r eca l l window was opened,
exposing
an
8-inch l ine without the
ci rc le
referent on i t .
The
subject
was
ins t ruc ted
to mark t h i s l ine
where
he
thought
the
ci rc le
should
appear ( i . e . the same
distance
from
the
l e f t
end of the
l ine) .
S was given 15 sec.
in which
to r eca l l
the
inspection stimulus and
then
a new
t r i a l
began. Retention was
tested af t e r three dif fe ren t in te rva ls , 6,
12
or 4 seconds.
For
half
of the t r i a l s a t each in terval (res t t r i a l s ) , the
subject was simply
instructed to
re s t
quiet ly with his
eyes
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38.
Figure
12
Posner Task: Experimental
Design
indicating
position mm) of test stimulus
from left
end of lin
Retention Interval seconds)
6 12
24
20
22
16
Rest
60
116
73
11
70
123
161
165
175
Intepolated Activity
38
45
50
Work
82
145
90
140
95
150
180
186
183
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Figure 13
Posner Test Appara tus
nspect ion
Recal l
39
-
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CORSI 40.
f ixa ted midway between
the
windows.
For
t he o the r
ha l f
work
t r i a l s ) ,
he was
requi red
to arrange
s t r ings o f 5 random d ig i t s
in cor rec t
ascending order .
wo
scores expressed in terms o f
the absolu te
dis tance
between
the
cor rec t l oca t ion
of the
c i r c l e
and the r eca l l ed pos i t i on were obta ined for each
subjec t .
One
score was t he t o t a l e r r o r mil l imetres) across
t he th ree r e t en t i on i n t e r va l s for t he r e s t condi t ion and t he
o the r was
t he
t o t a l
e r r o r
across
i n t e r va l s fo r the work
condi t ion .
To da te , 39
pat ien t s
with
r igh t
temporal - lobe exc i s ions ,
5 pat ien t s with l e f t temporal - lobe excis ions and 19 normal
con t ro l sub jec t s
have
been
examined on t h i s
t ask .
Mean er ror
scores fo r
the
r e s t and work condi t ions for
these
groups
a re
presented in Figure
14
As
pred ic t ed , the r i g h t temporal
pat ien t s show an impairment on t h i s
non-verbal r e c a l l t a sk
when
compared
with the l e f t
temporal
pat ien t s r e s t condi t ion ,
t
=
3.73,
P
.50) .
Mean er ror scores
for the
four
r igh t - tempora l sub-groups
a re given
in
Table 5
and
t h e i r performance as a funct ion o f
the r e t en t i on
i n t e rva l
i s i l l u s t r a t e d in Figure 15 for t he
r e s t condi t ion and in
Figure
16 for t he
work condi t ion .
In
the
work
condi t ion of
t h i s
t a s k , r e t en t i on was
progress ive ly
more
impaired as the
magnitude
o f
the
medial temporal - lobe
removal
increased . Those people with
the
hippocampus spared
in
the
r igh t
hemisphere Group
I )
and
pat ien t s
with only t he
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41.
CORSI
Figure 14
Recall
of
Visual Information
(Posner Task):
ean
Total
Absolute Error (mm) for Work
and
est Conditions
130 Rest Trials
Work
Trials
121 1
120
.
.
.
.
..
.
.
-
.
.
.
.
110
E
.
-
.
..
.
99.8
.
.
.
94.4
.
.
.
.
.
.
.
..
..
.
.
.
..
..
..
.
80
.
.
.
.
.
.
.
.
..
.
.
.
68.8
69.6
.
.
..
.
..
.
.
70
.
.
.
.
.
.
.
.
.
.
.
.
..
.
0 ~ ~ ~ ~ ~ ~
Normal Left Right Normal Left Right
Control Temporal Temporal Control Temporal Temporal
(N=19) (N=25) (N=38) (N=19) (N=25) (N=38)
roup
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42.
Table
5
Recall of Visual Information (Posner Task : Mean
Absolute Error
for
Right Temporal
Subgroups
Mean Error in mm
Group
N
Rest Trials
Work Trials
Left Tem pora
25
69.6 94.4
ight Temporal
7
93.7
99 1
ight
Temporal
14
83.6
110 4
ight Temporal
7
93.6
125.6
Right Tem poral V
1257
145.4
-
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43.
Figure 15
Recall
or Vllual
Position l a
Fundion of Retention Interval
for
Rest Condition
Corsi
version
of
Posner
Task
70
60
E
.
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44.
Figure 16
Recall of Visual Position as a
undion of Retention Interval for Work Condition
(Corsi version of Posner Task)
70
Right
Temporals
Group
4
60
E
E
II 50
o
~ a G r O U P
::
....
40
o
Group
2
...
o
'" Group
1
s ~ , - - - - - _ - - - : c : : - : - : - : - : - ~ : Left Temporal.
o
,'
t:: 30
w
.
,'
,'
-
Normal
",'"
o
Controls
....
20
c
o
Q
E 1
o ~ - - - - - - ~ - - - - - - ~ - - - - - - - - - - - - - - - - -
6 12 18 24
Time Interval (seconds)
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45.
pes hippocampi excised
(Group I I
did not show a s ignif icant
def i c i t when
compared
to the
l e f t
temporal pat ients
(Group
I
vs l e f t
temporals,
t =
0.25,
P >.50; Group
I I
vs l e f t temporals,
t
1.44,
P
>.25).
However,
the
pat ients in
Group
I I I
and
IV
with more radical excisions of the hippocampal region were
impaired
re la t ive
to
the
l e f t temporal group
(Group
I I I
vs
l e f t
temporals ,
t
2.00,
P
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46.
was somewhat bet ter than
his
reca l l of the non-recurring
digi t sequences (12 per cent , as noted
above).
This
severely impaired performance for both verbal and
non-verbal
learning
tasks
occurred
in sp i te
of his
normal immediate
span
for
digi t s (6)
and block patterns (5).
For
both
formally-similar
r eca l l tasks
H.M.'s
performance
was markedly impaired, and a t the longer re tent ion
in tervals
with interpolated
act iv i ty
the t e s t st imuli
appeared
to
exert
l i t t l e control
over his responses. Figure
17 shows tha t
his
reca l l
of consonant trigrams (Peterson task) was extremely
def ic ient not
only
re la t ive to normal control
subjects
but
even when compared
to
the l e f t temporal-lobe
pat ients
with the
most rad ica l
unilateral-hippocampal excisions.
Altogether
H.M.
reca l led
22.2
per
cent of
the
consonants
as compared to
47.7 per cent correct r eca l l
for
the
most
impaired l e f t temporal
group. To
assess
the immediate reg is t ra t ion of information for
t h i s
pa t ien t
four
t r i a l s
were
conducted
a t
zero
delay.
On
these
t r i a l s a
t r igram
followed
by
a
three
dig i t
number
was
presented (e .g . QZC465 )
and,
immediately the reaf te r H.M. was
requested to repeat
the
t r igram ("QZC"). For
th i s
condit ion,
he
correc t ly
recal led 100
per
cent of the
consonants. I t
should
be noted
tha t
the experimental
procedure
was
simplified
for
H.M.
because
of his
inabi l i ty
to
remember
the
original
t e s t ins t ruct ions .
On
each
t r i a l the
t e s t
mater ia l
was
read
aloud
to
him and he was required
to
count backwards unt i l
in terrupted by a gentle
tap on
the
shoulder
for reca l l of
the
consonants. Following six pract ice t r i a l s H.M.
remembered
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47.
Figure 17
Peterson Task: Verbal Recall
as a Function of Retention
Interval
1
Normal Controls
.....
....
ell ....
......
-
:::
....
c
8
........
c:::
0
.
--
......
:::
ell
........
c:::
Left Temporal roup IV
.....
U
0
...
U
~
-
6
~
c:::
Patient H M -
c
C
u
4
~
~
-
'0/\
."'.
...
...
2
0
~
U
0
0
I
~ f
0
3
6
9 12 15 18
Retention
Interval seconds)
-
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'+8.
without
prompting
on
a l l subsequent t e s t t r i a l s to
count
backwards and then, upon in terrupt ion, to attempt the r eca l l
of some
l e t t e r s .
Final ly , for the Posner task, he demonstrate
nearly
normal
reca l l a f ter
s ix
seconds
with
no
dis trac t ing
act iv i ty during the re tent ion in te rva l ,
however,
as indicated
in
Figure 18, his non-verbal r eca l l deter iorated very rapidly
as the delay period increased. For the work condit ion with
in terpolated act iv i ty during
the re tent ion
in te rva l , his
performance f e l l to a chance level ( i . e . as estimated by
the examiner - H.M.'s responses were
impar t ia l
re la t ive
to
the posi t ion
of
the t e s t stimulus) across a l l three delay
periods.
Discussion
The resu l ts of
the experiments
reported here
provide
fur ther
evidence
of hemispheric specia l izat ion of function.
The
outcome
for the two analogous short- term learning
t asks ,
the
Hebb
recurr ing-digi ts
t e s t
and
the
block-tapping
t e s t ,
demonstrates
a c lear double dissociat ion between
the
effects
of
l e f t
and r igh t temporal-lobe les ions . The l e f t
temporal
lobe
pat ients showed a def i c i t
for
the verbal
learning task
and normal
performance for
the non-verbal
analogue, whereas the
converse
was
evident
for the
r igh t temporal-lobe
patients .
This
same
pat tern
of
resu l ts
was
observed
for
the
two
formally
simi lar
t e s t s
of short- term r eca l l . These f indings are
consonant
with the corpus of
evidence
gathered from normal
and
cl in ica l
experiments tha t
demonstrate the
dif fe ren t
functions
of
the l e f t and r igh t
hemispheres in
the
mediation
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CORSI
49.
Figure 18
Recall of Visual Position as a
Function of Retention nterval
Corsi version of Posner Task)
300
Rest
---- Work
.
",'"
250
",'"
"
E
.
......... ",,,,,,,
"
'"
E
..... '"
Patient
H.M
""'..........
",'"
o 200
..... ",'" (Bilat. Hippoc.)
0 ::
.....
....
'.-
'
...
o
- 150
...
f
...
L I I
.2
o
100
....
c
o
Q)
_-----
... Right
Temporal
so
._-------
Group
4
.:.-.---- --------.
I C I
_----.------ Norma
ontro I
--
..
--
o
12
18
4
Time
Interval
(seconds)
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CORSI
50.
o f
human
behavior
see
Milner
1971) fo r the most recen t
review)
The
pr inc ipa l con t r ibu t ion o f the present study
i s
the
new f inding
t ha t
the sever i ty o f the mater i a l - spec i f i c memory
dis turbance
fol lowing
un i l a t e ra l
temporal
lobectomy i s d i rec t l y
r e l a t e d t o
the medial ex ten t
o f the
removal.
The more extens ive
the
surg ica l
encroachment on the hippocampal zone
in
the l e f t
hemisphere ,
the more severe
i s the
r e s u l t i ng
de f i c i t
in verbal
l ea rning and
re ten t ion .
Simi la r ly the sever i ty o f the
non
ve rba l
learn ing and
r e t e n t ion impairment
t ha t fol lows
r i gh t
temporal lobectomy
d i rec t l y depends on
the
extent of su rg ica l
removal in the r i gh t
medial temporal
region. The l e f t
temporal
lobe
p a t i e n t s
show normal performance
fo r
the
non-verba l
t a s ks
and the
r i gh t temporal - lobe
pa t i en t s show
i n t ac t
l ea rn ing and
r e c a l l of verba l mater i a l s rega rd less in each
group,
o f
the extent
o f
medial temporal
excis ion .
Although
the
hippo
campus
was
used
as the
brainmark
fo r de l inea t ing
the ex ten t
o f medial
temporal
removal, t i s not suggested t ha t t h i s i s
the so le s t ruc ture associa ted
with
t he memory dis turbances
t h a t have
been r epor ted . Rather , the e n t i r e medial aspect
o f
the temporal r eg ion inc luding hippocampus and parahippocampa
gyrus , i s taken to be assoc ia ted with the
observed impairments.
I t should
be pointed
out
t h a t
the two
ve rba l
tasks
employed
here
were presen ted in
the
aud i to ry mode, and t he
two
t e s t s
of
non-verbal performance were given in the v i sua l
mode. n argument could t he re fo re be
made
t h a t
se lec t ive
impairment i s
s pe c i f i c
in the
case
o f l e f t t empora l - lobe
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51.
damage, to the auditory modality, and,
in
the case of r igh t
temporal-lobe damage, to the
visual
modality.
At
present ,
there is indeed evidence
for a specif ic
defect
in acoustico
verbal
memory
following
l e f t
poster ior
temporal
or
temporo
par ie ta l les ions Luria, Sokolov Klimkowski, 1967; Warrington
Shall ice,
1969; Warrington,
Logue
Prat t 1971; Luria,
1971).
Nevertheless,
t seems unlikely tha t sense
modality is a c r i t i ca l
variable in the present studies. In cases of
l e f t an t e r io r
lesions
of the temporal lobe,
such as those
studied here,
a
select ive
impairment
in verbal memory
has been
consis tent ly
observed regardless
of
whether
the
material
i s heard or read
Blakemore Falconer, 1967; Milner, 1967). Furthermore,
recognition
and re tent ion of complex auditory patterns to
which a name
cannot be easi ly
given
is entire ly
normal for
pat ients with
l e f t temporal-lobe les ions, whereas people
with
r ight
ante r ior temporal-lobe damage show a
def ic i t
on
the
same
acoustic task
Shankweiler, 1966).
On
the basis of
th i s
evidenc
t can
be assumed
tha t the impairments reported here
were
mater ia l- ra ther than modali ty-specif ic .
The Patterri
of Memory Dysfunction
Before considering any
theoret ica l implicat ions
of
th i s
work, t i s necessary
to
describe more precise ly the pat tern
of mnemonic
dysfunction
tha t
emerges af ter
both
uni la te ra l
and
bi la tera l les ions
of
the
hippocampal
region. The
experiments
have
demonstrated
tha t immediate memory span
for
verbal
and non-verbal
information
was
in tac t in a l l cases.
The reg is t ra t ion of new information
seemed to
occur without
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52.
impedance. However the r e s u l t s fo r the two shor t - term
r e t e n t i o n
tasks Peterson and Posner
t e s t s )
revea led t ha t
pa t i en t s with
un i l a t e ra l
removals of the medial t empora l -
lobe
s t ruc tu res
were
unable
to
hold
i npu t s
fo r
even
very
shor t
i n t e rva l s , espec ia l ly when t he
oppor tun i t i e s
fo r
rehearsa l
were
r e s t r i c t ed .
Yet
fo r ne i the r shor t - term
t a sk , was
the re any sharp
d i scon t inu i ty
between the pe r
formance
o f people
with extens ive
medial
temporal - lobe
exc is ions and
t ha t
o f
normal
con t ro l
sub jec t s .
t i s unfor tuna te
t ha t
immediate r e c a l l a t zero delay
was not
formal ly inves t iga ted
for e i t he r of
the
shor t - t e rm
r e t e n t i o n
t a sks . Nevertheless ,
it
was
the
case t ha t
two
pre t r i a l s
a t
zero delay were presented as prac t i ce fo r the
Peterson t e s t and each
pat i en t ,
r egard les s of l e s ion s i t e ,
was able to
r e c a l l
cor rec t ly the
consonant
t r igrams under
t h i s cond i t ion .
As
pointed out e a r l i e r ,
the re
was
no
s igni f icant d i f fe rence
in immediate memory span
across
the
pa t ien t and
con t ro l groups and
t h i s f ind ing lends fur the r
suppor t to t he assumption
o f
i n t ac t r eg i s t r a t i on fo r
a l l
subjec ts . I f it i s assumed fo r the Peterson t a sk t ha t
a t
zero delay a l l sub jec t s were r e c a l l i ng
near ly
100
per cent
o f t he t e s t mater i a l , then , as ind ica ted in Figure 19 the
decay
func t ions
between
zero
and
t h ree
seconds
fo r
the
l e f t
temporal - lobe pa t i e n t s become
progress ively s teeper as the
medial
extent of
the
removal
inc reases .
The
primary l o s s
fo r pa t i en t s
with
r a d i c a l l e f t hippocampectomy
seems
to
occur
very
ear ly
i n the re t en t ion per iod; in f ac t ,
it
occurs
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CORSI
53.
Figure 19
Peterson
Task
Verbal
Recall as a
undion
of
Retention
Interval
100
0
u
Q)
90
a :::
u
80
n
-
)
-
0
70
c
U
-
0
en
60
c c
Q)
0
u
U
50
)
0
Q
40
0
30
Q)
I
I
I
I
I
0
0
3
6
9
2
15
8
Retention Interval