Human memory and the medial temporal region of the brain.pdf

8/9/2019 Human memory and the medial temporal region of the brain.pdf

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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


2/84

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


3/84

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


12/84

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


13/84

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) .


14/84

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


15/84

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


16/84

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


17/84

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


18/84

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


19/84

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


20/84

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,


21/84

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


22/84

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


23/84

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}


24/84

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


25/84

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


26/84

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


27/84

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


28/84

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


29/84

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


30/84

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


31/84

CORSI

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)


32/84

CORSI

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


33/84

CORSI

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


34/84

ORSI

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


35/84

ORSI

29.

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.


36/84

ORSI

30.

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


37/84

CORSI

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


39/84

CORSI

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)


40/84

CORSI

34

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


41/84

CORSI

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


42/84

CORSI

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


43/84

CORSI

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


44/84

CORSI

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


45/84

ORSI

Figure 13

Posner Test Appara tus

nspect ion

Recal l

39


46/84

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


47/84

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


48/84

CORSI

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


49/84

CORSI

43.

Figure 15

Recall

or Vllual

Position l a

Fundion of Retention Interval

for

Rest Condition

Corsi

version

of

Posner

Task

70

60

E

.


50/84

CORSI

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)


51/84

ORSI

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


52/84

ORSI

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


53/84

CORSI

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)


54/84

ORSI

'+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


55/84

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)


56/84

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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ORSI

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


58/84

ORSI

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


59/84

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

Human memory and the medial temporal region of the brain.pdf

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