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BRAIN A N D L A N G U A G E 2, 4 5 - 6 4 (1975)

Psychometric Studies of Verbal Functions Fallowing


Thalamic Lesions in Humans~

M A N U E L RIKLAN AND IRVING S. COOPER

Institute of Neuroscience, St. Barnabas Hospital

Psychometric studies following surgically induced thalamic lesions in humans


suggest that thalamic nuclei, in particular VL and pulvinar, play a role in verbal
functions, most specifically those involving fluency. The left thalamus tends to be
dominant in this respect, quantitatively rather than qualitatively, more in the na-
ture of a continuum than a dichotomy. Thalamic nuclei participate both in the
specific sensorimotor functions underlying verbal behavior and in the alerting or
arousal aspects of such behavior. Moreover, the thalamus interacts with cortical,
brain stem, basal ganglia, and possibly limbic systems in these functions. Longer
range postoperative alterations in verbal functions are ordinarily not observed due
to the availability of compensatory mechanisms and the presence of small lesions
within larger functional zones. The integrative level of tl~e preoperative brain is a
significant variable in predicting the presence or absence, and degree of post-
operative verbal alterations.

For the past two decades numerous psychological studies have been
undertaken of individuals subjected to thalamic lesions for the allevia-
tion of neurological symptoms. The vast majority of these were parkin-
sonians undergoing ventrolateral thalamectomy for the relief of tremor
and rigidity (cf. Cooper, 1968). More recently patients with other move-
ment disorders, and with spasticity or pain, secondary to stroke and
other neurologic disorders, were also assessed before and after pulvinar
surgery (Cooper, Amin, Chandra & Waltz, 1973). In most instances the
psychological studies involved pre- and postoperative administration of
standardized psychometric tests.
It is the purpose of this paper to review data derived primarily from
such psychometric studies of patients undergoing therapeutic thalamic
surgery, and to develop concepts on the role of the thalamus in verbal
behavior. Particular emphasis will be placed on the Wechsler Adult In-
telligence Scale (or Wechsler-Bellevue Intelligence Scale) since this par-
ticular test has been most frequently used, and it provides separate
"verbal" and "nonverbal" scores. This is specially useful in the frame-
work of this presentation since a proper assessment of verbal functions

1 Portions of the studies described in this report were supported by the Social and Reha-
bilitation Service of the Department of HEW, and The John A. Hartford Foundation, Inc.,
New York City.

45

Copyright © 1975 by Academic Press, Inc. Printed in the United States.


All rights of reproduction in any form reserved.
46 RIKLAN AND COOPER

is enhanced by a comparison of verbal and nonverbal functions. Nu-


merous other verbal and nonverbal tests have been utilized by various
investigators in this area, and will be considered at appropriate times.
Moreover, special comparisons will be made between the effects of left
and right hemisphere thalamic lesions and between ventrolateral and
pulvinar lesions. Such comparisons will provide data for a more articu-
late later consideration of the role of the thalamus generally, and of spe-
cific thalamic nuclei in verbal functions. The general design of most
studies under consideration involved preoperative, immediate postopera-
tive and follow-up psychometric testing of patients, with utilization of
control groups, when indicated. The details of such designs will be
delineated at appropriate times.
BACKGROUND

There now exists a fairly extensive body of literature on the psycholog-


ical effects of surgically placed lesions in various thalamic, particularly
the ventrolateral (VL), nuclei in man. Riklan and Levita (1969) have
recently reviewed the psychological consequences of lesions placed in
the VL nucleus in the parkinsonian. They noted, first, that the parkin-
sonian's preoperative level of behavioral and cerebral integration was
closely related to the degree of psychological alteration observed both
immediately postoperatively and in longer range postoperative assess-
ment. During the period immediately following VL surgery, a time
ranging from 5 to 21 days after surgery, losses in various integrative
functions were associated with both unilateral and bilateral lesions. Such
deficits were not necessarily related to a single anatomic structure but
seemed rather to reflect a general disruption of neural functions. In the
follow-up situation, 6 months or more after surgery, mean psychological
test scores generally return to their preoperative level. These findings
were interpreted as representing a lack of specific longer range behav-
ioral effects associated with unilateral and/or bilateral VL lesions and
were interepreted in the framework of cerebral plasticity and/or equipo-
tentiality. It was suggested that small lesions placed within larger func-
tional systems permit the remaining tissues to undertake the functions
involved. Finally, apparent lack of longer range effects might also reflect
psychometric test insensitivity to subtle "nonspecific" behavioral alter-
ations.
A number of clinical reports, largely those of neurosurgeons, have
dealt specifically with speech and language effects of VL lesions. Speech
difficulties during the first 2 weeks following surgery were reported by
Cooper (1961) for some 10% of patients undergoing unilateral chemo-
pallidectomy and chemothalamectomy. About 20% of these difficulties
were described as "aphasic" and were believed to follow surgery on the
VERBAL F U N C T I O N S A N D THALAM1C LESIONS 47

dominant hemisphere. They were usually found to improve within sev-


eral weeks. In contrast to unilateral intervention, bilateral basal ganglia
surgery appeared to threaten "speech" in a more enduring manner.
Among the first 100 consecutive patients with such operations, 18%
experienced some transient speech abnormality, with 6% having a
lasting handicap, which simulated the speech of pseudobulbar palsy. A
statistical tabulation of the sequelae for 1000 consecutive patients un-
dergoing cryosurgery for Parkinsonism (Waltz, Riklan, Stellar & Coo-
per, 1966) indicated that "speech" deficits occurred immediately after
surgery in 13.1% of patients. In the case of unilateral operations such
deficits again were described as transient, with indications of more
enduring alterations in the case of bilateral operations. Hermann,
Turner, Gillingham, and Gaze (1966) assessed dysphasia, dysarthria,
and voice volume in relation to stimulation and surgical lesions of the
basal ganglia in parkinsonians, and found dysphasia occurred only after
left-sided lesions in right-handed patients. The mean size of lesion in pa-
tients developing dysphasia was greater than the mean size of the total
group studies. Furthermore, pure capsular lesions did not result in
dysphasia, suggesting to these authors a subcortical mechanism for this
disturbance.
"A true disorder of language" of several weeks' duration was reported
after left pallidal surgery in one study (Svennilson, Torvik, Lowe & Lek-
sell, 1960), while transient "dysphasia" in some patients following left
hemisphere lesions was noted in another (Allan, Turner & Gadea-Ciria,
1966). Hartmann-von Monakow (1965) also described disorders of
expression, similar to cortically-produced aphasias, in Parkinsonian pa-
tients following diencephalic lesions. "Speech" impairments were re-
ported by Brain (1961) following stereotaxic operations on the globus
pallidus or thalamus for the relief of parkinsonism. According to Brain,
the corpus striatum may be more directly concerned with "speech" than
has hitherto been suspected, perhaps through its cortico-thalamic and
thalamo-cortical connections. In fact, substantial subcortical connec-
tions are clearly of major importance for the integration of speech
(Schuell, Jenkins & Jiminez-Pabon, 1964). And, in a symposium on
brain mechanisms underlying language and speech, Myers (1967) noted
that language disturbances may be seen with lesions of the thalamus.
However, such deficits cannot ordinarily be clearly defined, since pa-
tients with such lesions, usually tumors, manifest diffuse and severe
mental changes. Such findings led Lennenberg (1967) to state that "the
evidence is strong that language and speech are not confined to the cere-
bral cortex" (p. 64). In addition, changes in vocalization, particularly in
patterns of rate and rhythm, were observed following electrical stimula-
tion of subcortical structures in the course of stereotaxic surgery,
48 RIKLAN AND COOPER

lending further credence to the possible role of these areas in verbal


behaviors (Van Buren, 1963; Guiot, Hertzog, Rondet & Molina, 1961;
Schaltenbrand, 1965). Whether this role is purely motor in nature, e.g.,
articulation of symbols, or whether it involves the actual availability of
verbal symbols is not fully clear.
In contrast, slurring and stuttering in the absence of a "true aphasia"
was noted by Markham and Rand (1963) following unilateral subcortical
surgery of either hemisphere. Krayenbuehl, Akert, Hartmann, and Ya-
sargil (1964) also noted "speech" deficits in some patients following
lesions in the area of the ventrolateral thalamus, without involvement of
the internal capsule. However, "language" was not affected by such
surgery, according to these authors. After bilateral operations, slurring,
dysarthria, and decreased volume were also reported by Krayenbuehl,
Wyss, and Yasargil ( 1961).
Geschwind (1967) has questioned any role of the thalamus in
"aphasia." He would attribute language and speech deficits associated,
say, with a thalamic tumor, to pressure or edema which affect other
structures more closely related to these functions. Even following tha-
lamic surgery, Geschwind (1967) feels that patients may demonstrate
diminution in rate and volume of speech or may even become mute
rather than truly aphasic (p. 145).
Among the most articulate proponents of a possible thalamic contribu-
tion to language and speech have been Penfield and Roberts (1959), who
assessed such functions pre- and postoperatively in patients who suf-
fered mostly from focal cerebral seizures and who underwent temporal
lobe excisions, involving various amounts of neural tissue. In general,
according to Penfield and Roberts, the subcortical areas serve to coor-
dinate and to utilize the functional activies of cortical areas and to in-
tegrate such activities with those of the rest of the brain by means of
their projection fibers. Roberts and Penfield consequently proposed, as a
speech hypothesis, "that the functions of all three cortical speech areas
in man are coordinated by projections of each to parts of the thalamus,
and that by means of these circuits the elaboration of speech is somehow
carried out" (1959, pp. 207-208).
Recently, more direct data have become available concerning the ef-
fects of pulvinar lesions in man. The pulvinar is the largest thalamic
nucleus in man, and along with the dorsomedial nucleus, has undergone
the greatest phyletic expansion over the mammalian series. The prin-
cipal thalamic connections of the pulvinar are with the medial and lateral
geniculate bodies, lateral and central nuclear groups, and the dor-
somedial nucleus (Walker, 1966; Le Gros Clark & Northfield, 1937).
Papez (1939) has reviewed the evidence for connections with amygdala
and pyriform cortex. In addition, there are major reciprocal connections
VERBAL F U N C T I O N S A N D T H A L A M I C LESIONS 49

with the parietal cortex. The medial nucleus of the pulvinar projects
mainly to the posterior parietal region, and lateral nucleus to posterior
temporal lobe (Simpson, 1952; Truex & Carpenter, 1969). Van Buren
and Borke (1969) have suggested, on the basis of degeneration studies in
a few aphasic cases, that the anterior superior pulvinar is related to the
temporo-parietal speech area, In cats, evoked responses in the pulvinar
were noted following cutaneous stimulation (Richardson & Zorub,
1969). Kreindler, Crighel, and Marinchescu (1968) demonstrated re-
cently that, in cats, visual, auditory, and somatic afferents converge in
the same neuronal pools in the pulvinar-lateralis posterior complex
(PUL-LP). Such pools were found, also, to have projections to homolat-
eral and contralateral neocortical association areas. These authors
suggested that the P U L - L P complex is part of a large integrating
system, including the associative nuclei of the thalamus, the neocortex
(both associative and primary areas), and the thalamic nuclei of diffuse
porjection necessary to the modulation and control of the afferent
systems.

Psychometric Data
Detailed psychometric data of the effect of stereotaxic thalamic le-
sions on verbal: nonverbal functions is presented, first for ventrolateral
nuclear lesions, then for pulvinar.

THE V E N T R O L A T E R A L LESION

Initial psychometric studies of the ventrolateral thalamic lesion


through use of the Wechsler-Bellevue Intelligence Scale, indicated that
in the immediate postoperative status both left and right hemisphere
operates showed significant decreases in verbal and full-scale IQ scores,
but only the right hemisphere group demonstrated a significant decrease
in performance scores (Riklan, Diller, Weiner & Cooper, 1960). The left
brain operates, in contrast, showed significant verbal decreases and
small, nonsignificant performance increases. This represents an early
suggestion that left ventrolateral thalamic lesions may affect verbal func-
tions differentially.
Subsequently, pre- and postoperative change score data from patients
with left and right hemisphere ventrolateral thalamic lesions were sub-
jected to factor analysis (Riklan & Levita, 1964; Riklan & Levita, 1965).
These findings suggested that immediate postoperative change score pat-
terns consisted largely of similar factors irrespective of hemispheric
involvement, when verbal and nonverbal factors were compared. The
differences were largely in terms of factor loading: Greater verbal
loadings were noted for the left brain operates and greater nonverbal
loadings were obtained for the right brain operates. This relative absence
50 RIKLAN AND COOPER

of clearly defined qualitative verbal differences suggested then that such


functions may be subserved by neural processes inherent in either
and/or both hemispheres. It was then proposed that the concept of hemi-
spheric "dominance" may need qualification, at least with respect to
such subcortical structures as the thalamus. (See Table 1.)
In the course of further studies of verbal and nonverbal functions after
lesions directed to the VL thalamus, comparisons were made of the
psychometric effects of various lesion sites bordering on the ventrolat-
eral thalamus, in an effort to determine whether differential effects could
be noted. In an initial study (Levita & Riklan, 1965) cognitive and per-
ceptual functions of 22 parkinsonians were assessed following a unilat-
eral cryosurgical lesion placed in relation to the ventrolateral area of the
thalamus. It was found that verbal and spatial functions were not dif-
ferentially affected by antero-posterior, medial-lateral, and depth aspects
of the surgical lesion. Later, (Riklan, Levita, Samra & Cooper, 1969) the
relationship of number, size, and site of unilaterally and bilaterally in-
duced lesions in the area of the VL thalamus, to psychological changes
in parkinsonians was assessed. In no instance was lesion size or site,
within the general confines of the VL nucleus, significantly related to
cognitive changes, for verbally or nonverbally mediated tests. The "law
of physiological safety," the role of functional compensation, and the
presence of relatively small lesions within a larger thalamic zone were
noted in interpreting these results.
With respect to bilateral VL thalamic lesions, as compared to unilat-
eral lesions, cognitive functions measured through verbally and nonver-
bally mediated tasks were compared in parkinsonians undergoing no

TABLE 1
SUMMARY OF THE PRE-POSTOPERATIVE CHANGE FACTORS
(N = 71)

Left-brain Right-brain
variance variance
Change factors (%) (%)

Verbally mediated cognition 19 9


Nonverbally mediated cognition 13 19
Visual-motor construction expansion 12 12
Perceptual approach 11 12
Body image integration 11 12
Ideational productivity 9 9
Impulse control 9
Emotional reactivity 6
Perceptual integration - 9
Factors not identified 10 18

N o t e - f r o m Riklan and Levita (1964).


VERBAL FUNCTIONS AND THALAMIC LESIONS 51

surgery, unilateral right or left, and bilateral cryothalamectomy (Levita,


Riklan & Cooper, 1967). No significant differences obtained on any of
the behavioral dimensions for these four groups. Again, the possibility of
the contribution of a bilateral thalamic area was noted as possibly
explanatory of this lack of statistically significant differences.
In a more direct study of verbal behavior following thalamic lesions
(Samra, Riklan, Levita, Zimmerman, Waltz, Bergmann & Cooper, 1969)
the brains of 27 deceased parkinsonians who had undergone thalamic
surgery were examined anatomically to define the exact location of the
surgical lesion in each instance. A correlative study was then carried out
between the site of the lesion and any language or speech deficits which
may have resulted from the thalamic surgery. Language and speech were
assessed by two experienced speech pathologists who rated such speech
factors as voice quality, volume, rate and rhythm and language factors
such as adequacy of vocabulary, propositional speech, naming, counting,
repetition, and sentence usage. It was concluded that a lesion strictly
confined to the VL may be followed by language and/or speech deficits.
However, no definite relationship existed between postoperative lan-
guage or speech deficits and partial involvement of thalamic nuclei sur-
rounding VL nucleus, H fields of Forel, subthalamic nucleus or red
nucleus. Also, mild encroachment on the internal capsule could be
tolerated without language or speech deficits, so long as the pyramidal
tract remained intact. The size of the lesion was not related to post-
operative language and/or speech deficits. Postoperative language defi-
cits were mild and improved in time; whereas speech disturbances could
be either mild, moderate, or severe. When language deficits did occur,
they followed surgery on the left hemisphere in most instances. In con-
tradistinction, no definite relationship was found between the side of
surgery and speech deficits. Language and speech disturbances were
more frequently associated with bilateral rather than with unilateral
surgery, regardless of the cerebral hemisphere involved in the second
operation.
Further psychometric testing of verbal and nonverbal effects of left
and right VL thalamic lesions, respectively, was later undertaken using
another battery of verbal and nonverbal tests (Riklan & Levita, 1970).
The tests included the Stroop Word Color Interference Test (Stroop,
1935), the Graham-Kendall Memory for Designs Test (Graham & Ken-
dall, 1960; Graham & Kendall, 1947), the Odd Words Test (Holzinger
& Crowder, 1955), the Minnesota Paper Form Board (Patterson, Elliott,
Anderson, Toops & Heidbreder, 1930; Quasha & Likert, 1937) and
tests involving object naming and word fluency. These were adminis-
tered to a series of parkinsonians before and after left and right cryothal-
amectomy.
52 R1KLAN A N D COOPER

Differential performances were noted in the left brain, right brain, and
bilateral operates in several instances. Lateralized differences, most pro-
nounced in tests based on manipulation, creative retrieval and cat-
egorization of symbols, particularly word fluency and object naming,
showed the most pronounced effects of lesion laterality. For such tests,
left hemisphere operates revealed significant decrease in performance
immediately after surgery in the absence of such changes in the case of
right brain operates. In turn, bilateral operates also tended to perform
less well than unoperated control patients during the immediate post-
operative situation. Thus, in tasks of verbal fluency or verbal "flexibil-
ity," left brain surgery affects performance; so does a second side opera-
tion, regardless of laterality, whereas a unilateral right brain operation
did not have any such effects. Thus, verbal tasks of fluency or flexibility
yield a pattern of changes clearly associated with lesion laterality where
standard clinical tests did not (Riklan & Levita, 1964, 1969). Of further
interest is the fact-that a number of tests which may be described as
spatial-perceptual did not seem to differentiate between the hemisphere
groups to any degree. Specifically, the Graham-Kendall, Minnesota
Paper Form Board, identical pictures tests, and the Muller-Lyer Illusion
did not show any differences between the hemisphere groups at any time
postoperatively.
A multidisciplinary study was also undertaken to compare and con-
trast observations and assessments made by neurosurgeons, psycholo-
gists and speech therapists, with special reference to speech and
language correlates of the VL thalamic nucleus (Riklan, Levita, Zim-
merman & Cooper, 1969). The psychometric test battery included tests
of verbal fluency and articulation similar to those just described. While
findings must be considered preliminary and need of corroboration and
refinement, it was again observed that alterations of fluency, presence of
hesitations, and blocking in language may occur immediately after a left
ventrolateral thalamic lesion in right-handed patients. These changes
cannot be distinguished from dysphasia frequently described following
left-sided cortical lesions. When these alterations occur in patients
operated upon unilaterally, language functions return to the preoperative
level within several weeks after surgery.
Slight alterations in complex language may also occur after the place-
ment of unilateral right hemisphere thalamic lesions in right-handed pa-
tients. Such changes are ordinarily detected by tests of verbal crysta-
lized functions involving permutations of symbols and relations among
signs and symbols, rather than fluency. Findings based on such tests
revealed a lack of significant qualitative differences between left and
right thalamic lesions in this area, although quantitative differences are
present. A second-sided thalamic lesion may lead to a speech impair-
VERBAL FUNCTIONS AND THALAMIC LESIONS 53

merit in the nature of dysarthria. This is not a function of the laterality of


"second-side" surgery. The changes in VL thalamo-cortical connections
and their effects upon cortical outflows might be related to these defects.

THE PULVINAR LESION


In a preliminary study of language and cognition following surgical
lesions of the pulvinar in patients operated for the alleviation of pain and
spasticity (Brown, Riklan, Waltz, Jackson & Cooper, 1971), evaluation
of verbal or language behavior was undertaken through neuological as-
sessment, ratings by speech therapists, and through the administration of
psychometric tests, including the Wechsler Adult Intelligence Scale
(WAIS). From such assessments pre- and postoperatively, it was con-
cluded that individuals with normal preoperative language and cognition
can undergo unilateral right or left pulvinectomy without major alter-
ation in these functions during the immediate postoperative period.
Moreover, no alterations in constructional ability, calculation, right-left
orientation, reading, or visual imagery were observed. There was some
suggestion that mild defects in memory and/or verbal learning may
occur, but satisfactory control data are lacking.
Individuals with acquired preoperative deficits in language, or signs of
"organicity" on psychological tests, tended to show further regression
following unilateral pulvinectomy. These deficits, when present, ap-
peared in both verbal and nonverbal performance. As in previous studies
of VL lesions in parkinsonism and dystonia musculorum deformans
(Riklan & Levita, 1969), patients with intact "higher" functions can
withstand unilateral or bilateral surgical lesions in the thalamus, whereas
impaired patients often show further deterioration following surgery. It
is worth noting in this respect that the effect of cryopulvinectomy upon
language and cognition does not appear greatly different from that of VL
thalamotomy.
It must be stressed that interpretations of the pulvinar lesion data thus
far must remain tentative. Long range studies, further case material, and
lesion confirmation are necessary before definitive conclusions can be
reached. Further, it is essential to view these findings in relation to the
general effects of intra-cerebral surgery, and to surgical lesions of other
thalamic nuclei. Finally, the explorative nature of this study involved the
administration of a wide variety of rather standard clinical tests. It may
be that more subtle specific and refined test selection is necessary to
specify more precisely those linguistic and cognitive alterations which
may follow surgical lesions in the pulvinar.
In a more extensive psychometric study of pulvinar lesions in man
(Riklan, Weissman & Cooper, 1973) a battery of psychological tests
including the Wechsler Adult Intelligence Scale (WAIS), Wechsler
54 RIKLAN AND COOPER

TABLE 2
THE POPULATION--AGE, SEX, HANDEDNESS, DIAGNOSIS, LESION SIDE AND SITE

Lesion
Patient
No. Age Sex Handedness Diagnosis Side Site ~

1 51 M R Concussion, L PUL
Right Hemisphere
2 11 F R DMD L PUL
3 33 M R CP L PUL
4 45 M L Torticollis L PUL
5 41 F R CP R PUL
6 21 M R Epilepsy R PUL
7 13 F Ambidexterous DMD L PUL
8 10 F R DMD L PUL
9 29 M R CP R PUL
10 34 M R Athetosis R PUL
11 15 M R CP R PUL
12 56 F R Cancer L PUL
13 50 M L Right Spastic Hemiparesis L PUL
14 30 M L CP L PUL
15 38 F R CP with Torticollis R PUL
16 64 F R Intractable Pain R PUL
17 13 F R DMD R LP
18 52 F R CVA L LP & P U L
19 24 F L CP L LP & P U L
20 22 F R DMD L VL
21 13 F R DMD R VL
22 15 M L Post C V A - L e f t R VL
Hemisphere
23 13 F R DMD R VL
24 16 M R DMD L VL
25 60 M R Intention Tremor L VL & VPL
26 19 F Ambidexterous DMD L VL & VPL
27 44 M R PD L VL
28 16 M L DMD L VL
29 26 M L CP L VL & PUL
30 20 M L CP L VL & PUL
31 14 F R DMD L VL & PUL
32 16 M R CP R VL & PUL

N o t e - f r o m Cooper, Riklan and Rakic (1974).


a D M D , Dystonia Musculorum Deformans; CP, Cerebral Palsy; C V A , Cerebrovascular
Accident; PD, Parkinson's Disease.
b P U L , Pulvinar; LP, Lateral Posterior nuc.; VL, Ventrolateral nuc.; VPL, Ventro-
posterolateral nuc.
VERBAL F U N C T I O N S A N D T H A L A M I C LESIONS 55

Memory Scale, and Bender Visual-Motor Gestalt test were administered


to 32 consecutively tested patients who underwent VL or pulvinar
surgery. Data concerning the surgical technique and pathological confir-
mation of lesion placement has been presented elsewhere (Cooper,
Waltz, Amin & Fujita, 1971; Cooper et al. 1973). Table 2 presents data
on the population included in this study.
With respect to the WA1S sub-test scores, the question of verbal and
nonverbal effects of left and right pulvinar lesions, respectively, was of
particular relevance and data were tabulated for both pulvinar and VL
thalamic comparison subjects, to show the effects of left and right
thalamic surgery on verbal and performance portions of the psycho-
metric tests respectively. Table 3 presents these findings.
It is of interest to note that following right hemisphere lesions, for
either pulvinar or VL nuclei, no significant pre- to immediate postopera-
tive changes occurred either in verbal or performance tests of cognitive
and perceptual functions. However, left hemisphere operates, both pul-
vinar and VL, showed a differential effect with respect to verbal and per-
formance scores. Specifically, no changes occurred in performance tests,
whereas decrements in scores were noted for verbal functions following
left hemisphere surgery both for the pulvinar and VL operates. For the
VL lesion the pre- to postoperative changes were significant (p = .05),
based upon a one-tailed test of significance. For pulvinar lesions the
decrements showed a similar trend, but did not quite reach statistical sig-
nificance. Such data suggest a differential effect both of pulvinar and VL
lesions on verbal functions. I t is also of some interest to compare the
postoperative changes for this series of pulvinar and VL lesions with the
effects of VL and globus pallidus lesions noted in a larger group of
parkinsonians to whom a similar test was administered in an earlier
study (Riklan et al., 1960) in which a similar pattern of postoperative

TABLE 3
PULVINAR AND VENTROLATERAL (OR VL AND VPL) THALAMIC LESIONS
VERBAL-PERFORMANCE IQ SCORES--PREOPERATIVE AND IMMEDIATE
POSTOPERATIVE LEFT VS RIGHT THALAMIC SURGERY

Left hemisphere Right hemisphere

VIQ PIQ VIQ PIQ

Pre Post Pre Post Pre Post Pre Post

Pulvinar lesions
( N = 16) 99.2 89 78.1 77.5 92 92.2 80.5 82.7
Ventrolateral
lesions ( N = 9) 114.8 106.1 102 102.2 101.3 107.6 89 85.6

N o t e - f r o m Cooper, Riklan, and Rakic (1974).


56 RIKLAN AND COOPER

changes was noted. Specifically, during the immediate postoperative


state a general decline occurred, for the total group, in all of the sub-
tests under consideration. Statistical analysis of the individual sub-test
scores indicated that only the Digit Span and Digit Symbol sub-tests
were reduced significantly (p = .05). In long range testing all sub-test
scores had returned to their preoperative level.
When patients were separated into left and right hemisphere operates
the immediate postoperative and long range scores showed differential
alterations. The left hemisphere group demonstrated statistically signifi-
cant greater losses immediately postoperatively on the Digit Span, Simi-
larities, and Digit Symbol sub-tests (p = .05). These sub-tests involve
primarily verbal-symbolic responses with the possible exception of the
Digit Symbol sub-test, which requires perceptual-motor speed and accu-
racy. For right hemisphere operates the sub-test scores showing post-
operative decrements were Picture Arrangement, Block Design, and
Object Assembly, all requiring perceptual or perceptual-motor perform-
ance rather than verbal responses. None of these sub-tests was reduced
to a statistically significant degree. In longer range testing the right brain
operates had returned essentially to their preoperative status.
Perhaps the major difference between the pre- and postoperative test
scores for the later pulvinar and VL lesion group and the earlier VL and
globus pallidus group just noted for comparative purposes, is the some-
what greater decrements for the earlier group, immediately postopera-
tively, in both verbal and performance functions. It is quite possible that
this finding is related to the difference in the nature of the two samples.
The earlier sample included parkinsonians only whose mean age was 53
with an age range of 31-69 years. The later sample, pulvinar and VL
cases combined, includes a more heterogeneous group of patients whose
mean age is 29 with a range of 11-64 years. Among this group are many
younger individuals, particularly dystonics, whose brain and behavioral
functions might be described as more highly integrated than the older pa-
tients, and without structural damage. This factor will be considered in
further detail in the subsequent discussion.

A SYNTHESIS
Numerous psychometric studies are in substantial agreement that
surgically induced thalamic lesions tend to alter psychological functions,
including verbal performance during the immediate postoperative period.
This pattern has been confirmed by neurosurgical reports and assess-
ments by speech pathologists. In the longer range status, most aspects of
"integrative" psychological functions, including verbal performance, re-
turn to their preoperative level. Thus, concepts derived from assessment
VERBAL F U N C T I O N S AND T H A L A M I C LESIONS 57

of surgically induced thalamic lesions demand analysis of the acute post-


operative subject.
Within this overall pattern of immediate postoperative decrements in a
variety of psychological and behavioral functions, one special differen-
tiation obtains: Different degrees of postoperative alterations appear to
result from left- and right-sided lesions, whether the pulvinar or VL
nucleus is involved. Patients undergoing left thalamic surgery decline
more significantly in verbally mediated cognitive performance than those
undergoing right-sided surgery. In contrast, very few statistically signifi-
cant changes, either in verbal or nonverbal tests, occur in patients
having undergone right hemisphere surgery. This finding would seem to
confirm a number of suggestions concerning a thalamic role either in lan-
guage per se, or verbal test performance, and a tendency toward lat-
erlization of this function to the left hemisphere (cf. Penfield & Roberts,
1959; Riklan & Levita, 1969).
The immediate postoperative decrement in patients undergoing left-
sided operation is in a function best described as verbal fluency. Assess-
ments by speech therapists also suggest that some aspects of fluency are
correlated with left thalamic functions, confirming that the thalamus,
either the ventrolateral nucleus or nuclei functionally related to it, plays
a decisive role in some aspects of verbal formulation and expression.
Data on the pulvinar lesions are similar, but more tentative due to limita-
tions in numbers of patients studied.
Some other psychological tests of verbal behavior tend to show rela-
tively little differentiation between the effects of left and right brain
thalamic surgery. The verbal functions tapped by these standardized
psychological tests thus may be somewhat different from those involved
in "fluency," which may require a creative flexible approach to
searching and sorting. The fact that patients operated upon bilaterally,
who in most cases underwent right hemisphere operation for the second
side, showed changes similar to those undergoing left hemisphere
surgery in word "fluency" makes it apparent that the right thalamus also
participates in this function, at least in the presence of a previous lesion
of the left thalamus.
We have previously questioned the implied qualitative dichotomy
between left and right hemisphere functions (Riklan & Levita, 1964,
1965, 1969). A number of other investigators have proposed quantita-
tive gradations between the hemispheres, i.e., differences in emphasis
along a single continuum in the case of both hemispheres (Critchley,
1962; Eisenson, 1962; Hecaen, 1959; Wangwill, 1962). Recent studies
on split brain preparations (Gazzaniga, Bogen & Sperry, 1965; Gaz-
zaniga & Sperry, 1967; Sperry, 1961) have further underlined the im-
portance of interhemispheric relations. The assumed bilaterality of
58 RIKLAN AND COOPER

hypothetical "engrams" or memory traces would also stress the role


in interhemispheric relations in the integration and elaboration of infor-
mation (Ebner & Myers, 1962). Greater similarity may obtain between
the hemispheres than has been thought previously; future studies of
interactions may be more relevant than attempts to seek exclusive func-
tions for each hemisphere.
In the longer range situation mean verbal (and nonverbal) scores for
patients following either pulvinar or VL lesions, return essentially to
their preoperative status, as did those previously described for other
series of VL and globus pallidus lesions (Riklan & Levita, 1969). This
finding we have related to the fact that such surgical lesions ordinarily
involve only portions of larger zones of functional activity, and that suf-
ficient mechanisms of neural duplication and replication are available so
that no continuing functional deficit is manifest. As an example, in post-
mortem studies of three patients previously subjected to pulvinectomy,
lesions were typically described as including no more than half of the
nucleus, or less (Cooper, 1972). Current standardized psychological
tests also may not be sufficiently refined to discern subtle continuing
changes which might result from such lesions. Possible neural mecha-
nisms include plasticity or duplication of function within the thalamus or
the hemisphere which permit the re-establishment of integrated behav-
ioral patterns so that no continuing deficits remain in functional perform-
ance, and alternate mechanisms utilizing the other hemisphere. Finally,
the particular functions usually assessed may not be directly related to
VL or pulvinar zones.
Judging from results of testing pulvinar operates and several series of
Parkinson patients with bilateral subcortical lesions, it would appear that
such bilateral surgical lesions restricted to the globus pallidus, VL thal-
amus or pulvinar need have no significant lasting effect on cognitive-
perceptual functions whether verbally or nonverbally mediated. This
corroborates the clinical findings reported previously by others (Gill-
ingham, 1960-1961; Hassler & Reichert, 1958; Krayenbuehl, et al.,
1960; Krayenbuehl & Yasargil, 1961). Thus, while it is clinically appar-
ent, and data on length of hospitalization confirm the fact that second
side thalamic surgery involves a longer and more arduous immediate
postoperative course, a functional reorganization of "higher" integrative
behavior still occurs in due time.
With regard to neural concepts underlying thalamic-verbal interac-
tions, it has been generally established that the thalamus plays a critical
role in the relay of sensorimotor information, participates widely in af-
ferent and efferent integration, specific and diffuse, and is involved in the
elaboration of physiological data. Penfield and Roberts (1959, pp.
207-208) proposed that a bilaterally-distributed subcortical zone is
VERBAL F U N C T I O N S A N D T H A L A M I C LESIONS 59

responsible for the integration of speech. Changes in behavioral


"arousal," manifested by body movements and vocalization, have been
observed in Parkinson patients after repetitive unilateral stimulation in
the ventrolateral area of the thalamus (Schaltenbrand, 1965). Therefore,
stimulation or destruction of various points within the basal ganglia and
thalamus seems related to bilateral cortical responses and general behav-
ioral reactions involving the entire organism.
Alerting or arousal of the central nervous system is not just a function
of the reticular formation (Moruzzi & Magoun, 1949; Magoun, 1963).
The functionally-related nonspecific thalamo-cortical projections also
modulate bilaterally the sensorimotor functions of a wide area of cortex
(Jasper, 1949, 1960). The basal ganglia may exert a bilateral influence
upon ascending nonspecific activity and may be considered to be in-
tegrative centers as well (Martin, 1959; Krauthamer & Albe-Fessard,
1965). At the thalamic level, diffuse and specific neural systems inti-
mately interact in the elaboration of cognitive information, verbal and
nonverbal. Diffuse bilateral processes might contribute alerting or atten-
tion components while concurrent specific processes would contribute
more content-oriented information. At the thalamic level, the less com-
pletely organized data may require greater diffuse activity to achieve
elaboration.
If, for a moment, verbal (i.e., language) functions are viewed as an in-
teraction between direction and intensity of behavior, deficits in these
functions following subcortical surgery might be related to disturbed bal-
ance between specific and nonspecific physiological systems. Such rea-
soning would seem to contrast with concepts based on the direct or indi-
rect involvement of one or more cortical structures which have been
traditionally considered to be most directly associated with motor ex-
pression of speech and even symbolic formulation itself. One might
propose that the thalamic lesion, VL or pulvinar, acts upon the sen-
sorimotor pathways correlated with language functions at stages of infor-
mation processing where presumably organization may require greater
diffuse energizing activity for the achievement of further elaboration and
eventual output. In fact, according to some recent evidence, certain
thalamic nuclei, particularly the centromedian and parts of the ventrolat-
eral nucleus, contribute to the activation of pyramidal (i.e., cortical)
motor functions possibly related to speech (Buser, 1966; Hassler, 1966;
Purpura, 1967). Furthermore, even specific thalamic nuclei, such as the
ventrolateral and ventroposterolateral, have connections with cortical
zones, and the destruction of these nuclei might similarly be related to
facets of speech, particularly those components involving sensorimotor
functions necessary for articulation and fluency. It would thus follow
that a unilateral or bilateral subcortical lesion affecting either a specific
60 RIKLAN AND COOPER

or a nonspecific system could be related to language disturbances. Con-


cerning the participation of nonspecific systems, Roberts (1966) noted
that a vital aspect in "speech" function is the ascending reticular ac-
tivating system, which participates in focusing attention upon auditory
stimuli.
The arousal, alerting, or driving mechanism related to verbal functions
cannot be limited to any specific structure of either hemisphere. Since
physiological systems associated with behavioral arousal presumably
operate collaboratively and bilaterally at all afferent, efferent, and feed-
back levels, attempts at specifc anatomic localization (limited to a single
thalamic nucleus, for example) may be functionally irrelevant, and
perhaps, impossible. Instead, the intimate collaboration and liaison
between specific and nonspecific thalamic and basal ganglia systems on
the one hand and cortical systems on the other might account for lan-
guage and speech modulation and fluency. The contribution of behav-
ioral and physiological activation to language and speech might also be
analogous to Head's (1926) proposal that all "mental activities are inex-
tricably dependent upon a state of central nervous system 'vigilance' or
on a 'rise in dynamic level'" (Lashley, 1951). Moreover, one might also
reason that Jackson's (Taylor, 1958) description of "propositional" and
"emotional" speech stresses direction and arousal, respectively. Specifi-
cally, propositional speech may be thought to involve primarily direction
and to "arise" in the "dominant" hemisphere, whereas "emotional or
automatic" speech, which has been associated with an aroused and "less
cortically" controlled nervous system, could "arise" in either cerebral
hemisphere. Such an observation was more recently made by Serafe-
tinides and Falconer (1963).
We would suggest that those verbal deficits following VL and pulvinar
lesions, which may be described as "aphasic" are associated with tha-
lamic influences. Acute disruption of these orderly influences, as in the
immediate postoperative situation, would naturally affect thalamo-cor-
tical integrations essential to symbolic formulation. Thus, the organizing
qualities of "nonspecific" thalamic nuclei would appear to be critical.
Such nuclei contribute to timing and fluency, as well as activation. In
turn, the neural organizations associated with language appear to extend
over considerable areas of the brain and may be organized in temporal
and spatial patterns. Such systems cannot be limited to a single thalamic
nucleus any more than they can be restricted to a single cortical locus. If
this assumption is correct, the relatively rapid disappearance of post-
operative cognitive-perceptual, and language deficits, and even the ab-
sence of such deficits in many instances, may be associated with the
very limited interference of small surgical lesions within a large bilateral
zone mediating behavioral arousal. It would follow that the remaining
V E R B A L F U N C T I O N S A N D T H A L A M I C LESIONS 61

neural structures provide sufficient physiological concomitants for the


re-establishment of integrative patterns between the directional and ac-
tivating aspects of behavior necessary for language performance.

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