Download Cortical tongue area studied by chronically

Brain (1994),117,117-132
Cortical tongue area studied by chronically
implanted subdural electrodes - with special
reference to parietal motor and frontal
sensory responses
Eiichirou Urasaki,l tSumio Uematsu,l Barry Gordon2 ,3 and Ronald P. Lesser 1,2,3
Departments of INeurosurgery and 2Neurology, The Johns
Hopkins University School of Medicine and 3The Zanvyl
Krieger Mind/Brain Institute, The Johns Hopkins
University, Baltimore, Maryland, USA
Correspondence to: Ronald P. Lesser, Department of
Neurology, Meyer 2-147, The Johns Hopkins Hospital, 600
North Wolfe Street, Baltimore, MD 21287-7247, USA
Summary
Motor and sensory cortical tongue representations were ex­
amined in 40 patients }vith intractable seizures who underwent
chronic subdural electrode grid implantation. Tongue responses
were observed in a wide area 4.5 cm anterior and 3 cm posterior
to the central sulcus. The distribution of the responses was not
influenced by whether the responses were unilateral or bilateral.
In patients with fronto-parietal lesions, the tongue motor area
was located significantly more superior to the Sylvian fissure
and more anterior to the central sulcus than was the tongue
motor area ofpatients without organic lesion. Both motor and
sensory responses were found outside of the classic precentral
or postcentral area on the lateral surface of the cortex. Motor
responses (parietal motor responses ') could occur posterior
to the central sulcus and, rarely, sensory responses ('frontal
sensory responses ') were identified anterior to the central sulcus.
These paradoxical parietal motor and frontal sensory responses
were seen in 17 out of 40 (42.5 %) patients. Nine of these 17
patients had no organic brain lesion on MRI. Clinical factors,
such as patient's age, duration of seizures and cognitive
functions (IQ, word fluency score), did not influence the
frequency of the paradoxical responses. However, patients with
brain lesions showed a tendency to have associated paradoxical
responses (P < 0.05). In conclusion, paradoxical responses
are not uncommon in epilepsy patients, particularly in those
with organic lesions. The physiological and clinical implications
of the paradoxical responses are discussed.
Key words: epilepsy; cerebral cortex; brain mapping; subdural electrode; tongue
Introduction
Material and methods
Classically, motor representation for the tongue is regarded as
being fairly localized and centred -- 1 cm anterior to the central
sulcus, with little spread further anterior or posterior to the
central sulcus (Foerster, 1936a,b; Penfield and Boldrey, 1937;
Penfield and Rasmussen, 1950; Libet et al., 1964; Libet, 1973;
Uematsu et al., 1992b) . We utilized chronic subdural recording
electrodes to investigate whether this localization is affected in
patients with brain lesions, and whether more widespread
distribution of responses could be seen in normal behaving
humans.
The present study documents (i) the wide distribution of
tongue motor and sensory responses on the lateral surface of
the brain; (ii) the low rate of sensory response to electrical
stimulation; (iii) the existence of paradoxical responses, such
as parietal nlotor and frontal sensory responses.
Ethical approval was received from the joint committee of
clinical investigations of the Johns Hopkins Medical Institute
for this study and informed consent was given by all patients
participating in this study.
Details of the surgical technique, grid placement and cortical
stimulations are described elsewhere (Lesser et al., 1987;
Uematsu, 1992).
© Oxford University Press 1994
Patients and grid implant
Forty patients were selected fronl 58 undergoing stimulation
mapping as part of epilepsy surgery undertaken at the Johns
Hopkins Hospital. Eighteen patients were excluded because of
uncertain identification of cerebral sulci (four patients) or no
tongue responses obtained (14 patients). The 40 patients studied
118
E. Urasaki et al.
included 22 males and 18 fen1ales, ranging in age from 9 to
57 years (mean 25.4 ± 10.2 years). The patients were divided
into three groups: (i) patients without any organic lesion; (ii)
patients with a fronto-parietal lesion; (iii) patients with a
temporal lesion. There were 28 patients without organic lesions
(24 left, four right) and 12 patients with organic lesions (10
left, two right). The patients with organic lesion included seven
fronto-parietal lesions (four astrocytomas, two angiomas and
one cortical dysplasia) and five temporal lesions (two astro­
cytomas, two angiomas and one arachnoid cyst). Lesions were
judged present or absent based on the results of MRI and direct
intra-operative visualization.
Grid and stimulation study
The electrode grid consists of multiple electrodes, each with
a diameter of 3 mm with an area 2 mm in diameter on each
electrode exposed for contact with cortex. The centre-to-centre
inter-electrode distance is 10 Illill. Stimulation is delivered with
50 Hz, 0.3 ms duration pulses in 3 - 5 strains. Pulses were
generated by a Grass 12 or a Grass S88 dual channel stimulator.
In each stimulation procedure, the beginning stimulus intensity
is 1 mA and stimulus intensity increases by 0.5 -1 rnA
increments to a maximum of 15 rnA or to a level producing
after-discharges. Maximum stimulation intensity depends on the
observation of motor or sensory phenomena by testing personnel
or reported by the patient, or the occurrence of EEG after­
discharges, which were monitored during the test (Lesser et al.,
1987).
For a typical electrode stimulation study (in 35 out of 40
patients), an electrode pair was formed between two adj acent
electrode contacts in the anterior to posterior direction, usually
parallel to the Sylvian fissure (Figs 1 and 2). Stimulation was
delivered initially to consecutive adjacent pairs of electrodes.
When precise delineation of a critical sensorimotor area was
needed, additional testing was performed, using additional
electrode combinations in the region of interest (Fig. 2A). In
five patients, stimulation was given approximately in the
orientation of the central sulcus, i. e. in a superior-to-inferior
direction (Fig. 3A).
Location of electrodes
The location of the electrodes in relation to the main sulci and
cortical vessels was noted and photographed intra-operatively.
A con1posite brain diagram was made based on the intra­
operative photographs and postoperative radiological studies for
each individual patient. The central sulcus was determined by
choosing among the cortical fissures along a modified Rolandic
line. First, the conventional Rolandic line as described by Taylor
and Haughton (1900) was drawn and then the line was modified
by shifting 100 anterior to the conventional line (Fig. 1), since
the conventional Rolandic line was established using cadaver
brain, which has been shown to displace posteriorly -- 100 from
the pre-mortem position of the central sulcus artery seen in
angiography (Ring and Waddington, 1967). Using these two
lines as gross landmarks of the central sulcus, and with special
attention paid to pre- and postcentral sulci, which are often
interrupted or connected to other sulci, while the majority of
the central sulcus is continuous, the central sulcus was drawn
for each patient (Missir et al., 1989; Ono et al., 1990).
Compiling data
For each pair of electrodes stimulated, the cortical location of
a given response was chosen to be the electrode closest to the
central sulcus and Sy1vian fissure. When only part of a disc
electrode of the pair contacted (but did not cross) the central
sulcus, the closest electrode was said to be the location of the
response. However, when the electrode pair crossed the central
sulcus, the electrode located further away from the central sulcus
was used for statistical calculation. This electrode was used
because, when a tongue response was obtained by stimulation
of the pair of bipolar electrodes crossing the central sulcus, there
was a greater possibility that the point eliciting the response
was included in the stimulated area of larger volume. We
separated these two categories of electrodes (touching or
crossing the central sulcus) and did not use them for analysis
of sensory responses in the frontal region and motor responses
in the parietal region, because they could possibly stimulate both
precentral and postcentral gyri.
The cortical area was divided into 1 x 1.5 em zones,
delineated by lines paralleling the Sylvian fissure and falling
1 em apart, as well as lines paralleling the central sulcus and
falling 1.5 em apart. The number of responses was counted
in each zone. Stin1ulation using a distant inactive reference was
not utilized because of time considerations, but we recognize
the possibility of some ambiguity concerning the electrode from
which the actual response was obtained in certain cases.
In some patients, individual electrodes were combined into
more than one bipolar pair (Figs 2A and 3A). If there was
uncertainty about stimulus response on a particular electrode
contact during serial additional stimulation, the response was
not counted in the statisticentral sulcus. For example, stimuli
to electrodes BI-Cl, Cl- Dl, Dl- El and El- Fl in Fig. 2A
elicited motor responses. Since no response occurred with
stimulation of Al - Bland F 1- G 1, we could conclude that
responses to stimulation of B1- C 1 and E 1- F 1 had to be due
to effects at C 1 and E 1, respectively. The D 1 electrode was
not counted as a response site, however, because we could
neither prove nor disprove D 1 as an origin of the motor response
elicited. These procedures certainly underestin1ate the number
of responses and the extent of the response distribution, but
they can be compared with the results obtained from mono­
polar stimulation (Penfield and Boldrey, 1937; Penfield and Ras­
mussen, 1950; Picard and Olivier, 1983; Luders et al., 1987)
and bipolar electrodes separated by < 1 cn1 (Libet et al., 1964;
Libet, 1973).
Responses were defined as (i) motor arrest (stopping of
voluntary rapid alternating tongue n10vements); (ii) motor
response (localized involuntary movement, pulling back or
twitching of the tongue, in response to cortical stimulation);
Sensory-motor cortical tongue representation
1
Fig. 1 Location of the electrodes on the implanted grid is shown. After tracing cortical sulci and gyri,
as determined from intraoperative photographs, on lateral skull X-ray films, the Rolandic line is
measured by the original method of Taylor and Haughton (1900), and a line 10° anterior to the original
line also is drawn. In this patient, the central sulcus is located between the two lines. (Electrodes on the
inferior temporal lobe and temporal base are not shown.) The patient was a 36-year-old, right-handed
man, with left-dominant hemisphere as determined by the Wada test, a verbal IQ of 111, performance
IQ of 92, full-scale IQ of 101, and word fluency score of 7.7. Seizure onset was at age 15 years. His
MRI and CT scan were normal. Left temporal seizure focus was detected. Open circles indicate disc
electrodes that did not elicit tongue responses; filled circles indicate electrode locations where motor
responses were elicited. A small filled circle in a square means a mixed response. Thin lines connect
two electrodes that evoked no tongue responses. Thick lines between electrodes indicate an electrode
pair that evoked some tongue responses. The location of a given response is chosen to be the electrode
closest to the central sulcus, e.g. G I in G 1- HI, 02 in C2 - 02, 03 in C3 - 03, and E3 in E3 - F3 of
bipolar electrodes. Electrode pairs E I - F I and E2 - F2 cross the central sulcus (CS) and because the
division of the inter-electrode line, as divided by the central sulcus, is larger from the central sulcus to
E I and E2, these sites were selected as the stimulus locations. Results from cortical stimulations are as
follows. AI-BI (15 rnA), no response; CI-DI (14 rnA), deficits in comprehension, reading passages,
reading single words, responsive naming and spontaneous speech; E 1- F I (3 rnA), tongue pulled in and
unable to speak; GI-HI (10 rnA), tongue pulled in and jaw twitch to right side, deficit in reading a
passage; A2-B2 (10 rnA), no response; C2-D2 (14 rnA), tongue pulled in; E2-F2 (6 rnA), tongue
pulled in, jaw pulled to right and unable to speak; G2 - H2 (12 rnA), no response; A3 - B3 (15 rnA),
no response; C3-D3 (15 rnA), tip of tongue curled up and deficit in reading passages; E3-F3
(II rnA), tongue pulled in and bilateral tongue sensation; G3-H3 (15 rnA), deficits in all speech and
language functions; from A4- B4 to G6- H6 (10-15 rnA), no response.
119
120
E. Urasaki et al.
Fig. 2 Tongue responses obtained from four patients without organic lesion. A square indicates an electrode where a sensory response
was elicited. An X-n1ark in an open circle means tongue motor arrest response. Other symbols are the same as in Fig. 1. A~ example of
parietal motor response is shown. Stimulation of electrode pairs D 1 - Eland E 1- F 1 produced tongue motor responses (pulling to right) ~
as well as right thumb twitching and a tingling sensation behind the right side of the lips and teeth. In this case, grid sizes were 6 x 8
over the lateral convexity ~ 2 x 8 underneath on the basiomesial temporal lobe and 4 x 5 over the frontal pole of the left language-dolninant
hemisphere. The patient was a 19-year-old left-handed man with complex partial seizures. The Wada test showed that the language areas
were represented bilaterally. The MRI scan was negative for the organic brain lesion. B l-C 1, tongue and jaw pulls to right~ and right­
hand finger nloven1ent stops~ C 1- D 1 ~ same as above; A2 - B2, tongue pulls in, right fingers bend at first knuckle, deficit in reading
phrase and comprehension; B2 -C2~ tongue n10ven1ent stops, mouth and jaw open, right finger movement stops; C2 - D2~ tingling on tip
of tongue, tongue pulls to right. jaw pulls to right~ right finger movement stops; D2 - E2, tongue pulls to right, jaw pulls to right,
tingling on right side of jaw; E2 - F2, tongue pulls to right, mouth pulls to right, tingling in right side of mouth; C3 - D3. tongue pulls
in; D3 - E3~ tongue pulls in~ jaw pulls down; E3 - F3, tingling in tongue on both sides. B~ example of frontal sensory response. Upon
stimulation through electrode pair C3 - D3 ~ the patient reported tingling on the right side of the tongue. The D3 electrode contact is
located just anterior to the central sulcus. (The diagram shows only the main 6 x 8 grid over the left language-dominant hemisphere.) The
patient was a 23-year-old won1an with the diagnosis of refractory seizure disorders. The MRI scan was negative for this organic brain
lesion. C 1- D 1, tongue retracts, mouth pulls to right, deficit in spontaneous speech; E2 - F2, tingling on the right side of tongue~ tongue
pulls to right. c, a 24-year-old, right-handed woman with complex partial seizures. The Wada test showed bilateral representation of the
language area. Mixed motor and sensory response was seen beyond the line 3 cm superior to Sylvian fissure (FI)~ which also implies
the existence of frontal sensory response. El- FI, right side of tongue and mouth twitch and tingle, right thumb tingles; C2 - D2~ tongue
pulls in, can~t talk; E2-F2~ tongue pulls in, can~t talk; C3-D3, tongue movement stops, mouth and jaw pull to right~ can't talk;
E3 - F3. tongue pulls in and tingle occurs bilaterally. D~ a 22-year-old man with temporal lobe epilepsy. Left language-dominant
hemisphere. In the temporal lobe ~ one motor arrest (D3) and one motor response (D4) were elicited. C 1- D 1, right tongue and facial
twitching; El- Fl, tongue pulls back, right n10uth opens, right lip twitches, right finger movement stops, right hand tingles; C3 - D3.
tongue movement stops~ mouth and jaw pull to right, right finger moven1ent stops, left throat tingles; E3 - F3, tongue pulls in~ C4 - D4.
tongue pulls back.
Sensory-motor cortical tongue representation
121
Fig. 3 Tongue responses obtained from two patients with organic lesions. Shaded areas indicate the lesions, as revealed by sagittal MRI
scan. A. a 36-year-old woman. left hemisphere dominant for language, with seizures secondary to left prefrontal cavernous angioma.
Although they were part of a mixed response, two frontal sensory responses were seen (E5 and E7). Tongue motor responses were also
obtained more than 4 cm superior to the Sylvian fissure (E4, F4). E3-E4, tongue pulls to right; F3-F4, tongue pulls to right; E2-F4,
tongue pulls to right. right side of face pulls to right; 05 - E5, tingling in right side of tongue, jaw and cheek, tongue pulls to right;
E5-E6. tingling on right side of tongue, numbness on right side of jaw, tongue pulls to right; C6-06, tongue pulls to right. 05-06,
lOngue and face pull to right; F5 - F6. tingling on the tip of right side of tongue. tongue pulls to right, right side of mouth twitches;
G5 - G6. tongue movement stops, right side of jaw twitches; 07 - E7, tongue pulls to right, bilateral tongue tingle; E7 - F7, same as
07-E7: F7-G7. same as 07-E7. B, a 22-year-old man, left hemisphere dominant for language, with seizures secondary to a low­
grade astrocytoma in left franta-parietal region. Motor and sensory responses were seen above the line 4 cm superior to the Sylvian
fissure. but no paradoxical responses were obtained in this case. EI-FI, tongue and mouth pull to right; C2-02, tongue pulls to right;
G2-H2. tingling in right side of tongue and lip.
(iii) sensory response (such as distinct tingling and numb­
ness): (iv) mixed response (simultaneous motor and sensory
responses). Awareness of tongue movement was not included
as a sensory response in this study. Discrete tongue sensation
localized in the tongue ipsilateral to the side of stimulation was
not included in this study since this is likely to be of trigeminal
origin (Lesser et al., 1985). The location, number and rate of
responses were examined and statistically analysed (Student's
non-paired t test, XC test, Fisher's exact test, McNemar's
test and multiple comparisons with Bonferroni's correction)
(Armitage, 1971; Itho, 1984; Tanaka and Tarumi, 1986).
Results
Tongue response
In the 40 patients, a total of 586 electrode pairs were placed
over the lateral convexity, within the cortical area from Sylvian
fissure to 5 cm superior to the Sylvian fissure and from 4.5 cm
anterior to 4.5 cm posterior to the central sulcus. Patients
included both those with and those without organic lesion. One
hundred and thirty of 586 electrode pairs (22.2%) produced
tongue responses. Seventy of the 130 (53.8%) were motor
responses, 26 (20%) were motor arrest, 23 (17.7%) were mixed
responses, and II (8.5%) were sensory responses.
In patients without organic lesion, 88 tongue responses were
obtained: 48 (54.5%) motor, 19 (21.6%) motor arrest, 15
(17.1 %) mixed and six (6.8%) sensory. The remaining 42
tongue responses were obtained from the patients with organic
lesions in either fronto-parietal or temporal regions.
Corlical tongue response in relation to central
sulcus
In patients both with and without organic lesion, 57 out of 70
(81.4 %) motor responses were observed anterior to the cen­
tral sulcus (frontal lobe). The remaining 13 (18.6%) motor
responses were observed posterior to the central sulcus (parietal
lobe) (Figs I and 2A). With regard to sensory responses, seven
out of II (63.6%) were located posterior to the central sulcus
and the remaining four (36.4 %) were observed in the frontal
lobe, anterior to the central sulcus (Fig. 28). Seventeen (65%)
of the 26 motor arrest responses and 14 (61 %) of the 23 mixed
responses were observed in the frontal lobe anterior to the
central sulcus.
In patients without organic lesion, 39 out of 48 (8 1%) motor
responses were anterior to the central sulcus and the remaining
nine (19 %) were observed posterior to the central sulcus
(Table IA). Of the sensory responses, five out of six (83%)
were located posterior to the central sulcus and the remaining
one (17 %) was anterior to the central sulcus. Twelve (63 %)
of the 19 motor arrest responses and eight (53 %) of the 15
mixed responses were observed in the frontal lobe (Table IA).
122
E. Urasaki et al.
Extent of cortical tongue representation
(c) Tongue responses in patients with temporal lesions
In all patients, with and without organic lesion, the tongue
responses were distributed along a 7.5 cm anterior-to-posterior
segment (4.5 cm anterior to the central sulcus and 3 cm posterior
to the central sulcus) (Table lA -e).
Frontal
Parietal
-­
~-
A
M
X
S
0
8
0
0
A
M
X
S
0
4
0
0
(40)
(22)
--­
Table 1 (A - C) Distribution of tongue responses by type
in patients without organic lesions (A), with fronto-parietal
organic lesions (B) and with temporal lesions (C)
- - - ­ FRONTAL AREA
+4.5an
A
~
PARIETAL AREA
+3.0
X
S
A
+1.5
CS
~~-F-~
X
-1.5
SAM
X
-3.0
S
M
X
-4.5
~
S
X
S
(A) Tongue responses in patients without organic lesions
Frontal
12
39
(1)
Parietal
(0)
(1)
8
(148)
-
1
-
-
-
-
-
(0)
-
-
-
-
-
-
-
1
-
(3)
1----
b
FRONTAL AREA
PARIETAL AREA
-----f-----
-
A
It!
+3.0
X
S
A
cs
+1.5
It!
S
X
A
M
X
S
-1.5
A
M
S
X
-3.0
A
M
X
-4.5
A
S
M
X
S
(4)
-
2
-
-
3
-
-
1
-
(3)
(3)
+4.5an
-
-
(4)
(1)
(0)
(0)
(2)
(1)
(1)
(0)
(3)
(4)
-
(0)
-
1
-
-
2
-
(7)
(3)
(4)
(5)
-
(0)
(3)
-
-
-
1
(4)
-
(3)
(0)
-
-
-
(II
SF
(0)
(5)
1
(7)
(0)
(2)
(10)
(4)
(4)
1
2
1
2
I
9
3
11
1
3
(9)
(l)
1
(10)
(1)
---~--
1
3
2
3
I
(22)
(16)
I
2
I
4
2
(27)
(5)
(22)
(2)
_ ..
-
(18)
3
(25)
I
(27)
2
(34)
2
­
I
(30)
2
I
2
9
(16)
I
2
(16)
(2)
(19)
(3)
2
4
(33)
(31)
SF
(B) Tongue responses in patients with fronto- parietal lesions
Frontal
A
M
5
10
Parietal
X
S
A
M
X
S
6
3
2
0
2
2
(86)
(37)
----~--
~._--------
FRONTAL
I
AREA----~--+----
PARIETAL AREA
b
+4.5an
A
M
+1. 5
+3.0
X
SAM
X
-
-
I
(6)
-
1
I
-
I
­
-
2
-
-
SF
­
1
-
­
-
-
1
~---~
-
-
(3)
1
1
1
­
-
-
I
3
I
­
-
-
-
1
­
-
-
-
1
M
XS
(1)
(0)
(1)
(0)
(4)
(l)
-
(5)
1
-4.5
A
1
1
(8)
1
XS
(3)
(6)
-
-3.0
SAM
(3)
-
(6)
(5)
-
X
(9)
I
1
SAM
I
(7)
(4)
(5)
3
(4)
(8)
-
I
X
(6)
(3)
-
­
-1. 5
CS
SAM
­
-
-
-
(4)
-
(6)......I...
-
-
(6)"""'
1
(4)
""""
-
-
-
(3)
---.J
For each table: A = total number of tongue responses in patients
without organic lesions, by type; B = cortical tongue responses,
distance from central sulcus (CS) and Sylvian fissure (SF), in
centimetres. Upper numbers in each column indicate the number
of responses per electrode pair. Lower numbers in parentheses
represent total electrode pairs at that cortical segment. For
exan1ple, in A, at the cortical segment 3 -4.5 em anterior to the
central sulcus and 3 -4 cm superior to the Sylvian fissure, there
is a motor arrest (A) response upon stimulation of seven electrode
pairs. In the inlffiediately posterior segment (1.5 - 3 cm anterior
to the central sulcus and 3 -4 em superior to the Sylvian fissure),
two motor arrest (A) responses and one mixed (X) response were
produced out of nine electrode pairs. There were no motor (M)
or sensory (S) responses at that location. The area outlined with a
thick line indicates the zones where tongue responses were
elicited.
With regard to distribution in relation to the Sylvian fissure,
the cortical area for tongue responses extended to as much as
4 cm superior to the Sy1vian fissure in patients without organic
lesion and to as much as 5 cm superior to the Sylvian fissure
in the patients with fronto-parietal lesions (Table 1A and B).
In patients with temporal lesions, only motor tongue responses
were obtained, and they were found within 3 cm superior to
the Sylvian fissure (Table Ie).
Tongue response rate and distribution
Patients without organic lesion
Rate of tongue responses (percentage of electrode pairs
producing tongue responses) upon stimulation of all electrodes
in each 1 x 1.5 cn1 area was calculated, as shown in Table 2.
In patients without organic lesion, the highest rate (%) of motor
response was found in the 1.5 cm area immediately anterior
to the central sulcus and I - 2 cm superior to the Sy1vian fissure
Sensory-motor cortical tongue representation
(Table 2A). At that site, 11 out of 27 electrode pairs (41 %)
produced tongue motor responses (Tables 1A and 2A). The
second and third most frequent locations were immediately
above and below the first site. Immediately above, 33 % of the
electrode pairs (nine out of 27 pairs) produced motor response,
and immediately below, 27 % (nine out of 33) produced motor
response. Although the numbers are noticeably smaller, there
were motor responses posterior to the central sulcus. For
example, a 13 % response rate (four out of 30) was found at
the area 0 - 1.5 em posterior to the central sulcus and 1- 2 em
superior to the Sylvian fissure, and a 6% response rate (one
out of 16) was found further posteriorly (Table 2A).
A relatively higher sensory response rate was found posterior
to the central sulcus and 0 - 1 or 2 - 3 em superior to the Sylvian
fissure (Table 2A).
Tongue motor arrest tended to be found toward the vertex,
further away from the Sylvian fissure. The higher rate of
response was noted 3 - 4 em superior to the SyIvian fissure.
In relation to the central sulcus, the majority of the motor arrest
responses were seen anterior to the central sulcus (Tables 1A
and 2A). A higher rate of mixed responses appeared to be
located around a 1.5 em zone both anterior and posterior to
the central sulcus (Table 2A).
Patients with organic lesion
Compared with the patients without organic lesion, patients with
fronto-parietallesions demonstrated tongue motor and sensory
response rates that tended to be higher at sites more anterior
to the central sulcus and more superior to the Sylvian fissure
(Table 2B). In patients with temporal lesions, motor responses
tended to be distributed 0-1.5 em anterior to the central sulcus,
a distribution similar to that in patients without organic lesions
(Table 2c).
Statistical analysis of the distribution of
responses
Relation to central sulcus and Sylvian fissure. To find
out whether there is a significant difference among cortical sites
for the different types of tongue responses, particularly in
relation to the central sulcus and/or SyIvian fissure, Student's
t test with Bonferroni' s correction for multiple comparison was
performed (Table 3A and B). In patients without organic lesion,
the mean location of motor responses, 0.77 ± 0.93 em anterior
to the central sulcus, was compared with the mean location of
sensory responses, 0.83 ± 0.72 em posterior to the central sulcus
(P < 0.001) (Table 3A and B). There was no significant
difference between the motor and sensory sites in relation to
the Sylvian fissure (Table 3B). For the motor and motor arrest
sites, there was no statistical difference in relation to either
central sulcus or Sylvian fissure. However, motor arrest sites
were significantly nlore anterior to central sulcus when com­
pared with sensory sites (P < 0.005) (Table 3B).
Cortical sites for nlixed responses tended to be closer to the
123
central sulcus than were motor response sites (P < 0.05)
(Table 3A and B). There was no apparent statistically significant
difference in the distance from the central sulcus or the Sylvian
fissure for nlotor versus motor arrest, mixed versus sensory,
or mixed versus motor arrest responses (P > 0.05) (Table 3A
and B).
Of the 48 nl0tor responses in patients without organic lesion,
two types of responses were noted; namely, pulling back with
no laterality on 32 occasions and lateral tongue deviation on
16 occasions. There was no apparent statistical difference in
their relationship to the central sulcus or the SyIvian fissure
(Table 4). Similarly, there was no significant difference between
bilateral sensory and unilateral sensory responses in relation
to the central sulcus or Sylvian fissure (Table 4).
Response rate. Response rates upon stimulation of all the
electrode pairs in a given square area of the frontal versus
parietal lobes were compared in patients without organic lesion.
There were 253 electrode pairs in the frontal lobe (anterior to
central sulcus) and 148 electrode pairs in the parietal lobe
(posterior to central sulcus), as shown in Table lA. Upon
stimulation of the electrode pairs in the frontal lobe, 60 electrode
pairs produced at least one response: motor, sensory, arrest
or mixed, a response rate of 23.7 % (Table 5). In the parietal
area, 28 out of 148 electrode pairs (18.9 %) produced some sort
of response. Although the frontal area has a higher response
rate than the parietal lobe, X2 testing showed no significant
difference.
When the motor response rate was analysed in frontal versus
parietal areas, the response rate for motor responses alone was
significantly higher in the frontal area (P < 0.01). Similarly,
the sensory response rate was significantly higher in the parietal
area (P < 0.05). For nlotor arrest and mixed responses, there
were no statistically significant differences between the electrode
pairs in frontal versus parietal lobes (Table 5).
When the sensory response rate was compared with the motor
response rate using McNenlar's statistical test (Armitage, 1971),
the sensory response rate was significantly lower in the
combined frontal and parietal area and in the area anterior to
the central sulcus (frontal) alone (Table 5). However, in the
parietal region, no statistically significant difference between
sensory response and motor response was obtained (McNenlar's
test) .
Location of organic lesions
Among the 12 patients with organic lesions, seven patients had
lesions in fronto-parietal areas. Four of the seven patients had
space-occupying lesions in the vicinity of the central sulcus.
In one of these patients, tongue motor response was recorded
4-5 em superior to the Sylvian fissure (Fig. 3B).
The remaining three with fronto-parietal lesions had non­
space-occupying lesions. Two of these were small (1.5 x 2 em
and 0.5 X 1 em) prefrontal angiomas detected by MRI and
confirmed histologically. In one of the patients with angioma,
124
E. Urasaki et al.
two motor responses were observed in the area 4 - 5 cm superior
to the Sylvian fissure (Fig. 3A). The remaining patient with
fronto-parietal lesion had dysplastic change in the prefrontal
lobe. Tongue motor response and arrest, one each, were found
4.2 and 4.5 cm superior to the Sylvian fissure, respectively.
The renlaining five patients had organic changes in the
temporal lobe away from the fronto-parietal area. Two patients
had angiomas, another two had a previous history of anterior
temporal lobectonly for low-grade astrocytoma, and the last
patient had a postoperative pseudocyst caused by posterior
temporal lobectomy for low-grade astrocytoma 10 years earlier.
Tongue responses were found 1- 3 cm from the SyIvian fissure
in all these patients.
Distances from the central sulcus and Sylvian fissure of each
tongue response in the patients with organic lesions were
compared with those of the patients without organic lesions
(Table 3A). Statistically, the tongue motor area of patients with
fronto-parietal lesions was located significantly more superior
to the Sylvian fissure (P < 0.001) and more anterior to the
central sulcus (P < 0.05) than that of patients without organic
lesion. There were no significant differences in the distances
for motor arrest, sensory and mixed tongue responses between
the patient groups. In patients with temporal lesions, only motor
responses were obtained, but the distances of the responses
from the Sylvian fissure and central sulcus were not signifi­
cantly different from those of patients without organic lesion
(Table 3A).
Tongue responses in the superior temporal gyrus
There were almost no tongue responses of any type outside the
brain area outlined in Table 1, namely > 5 cm superior to the
Sylvian fissure (67 electrode pairs studied) and > 4.5 cm
anterior or posterior to the central sulcus (56 electrode sites).
The exceptions were the three tongue responses found outside
the area; they occurred upon stimulation immediately inferior
to the Sylvian fissure, in the vicinity of the superior temporal
gyrus in two patients, one with a prefrontal angioma (0.5 x
1 cm) and the other with no MRI-demonstrated organic lesion
(Fig. 2D). One patient, a 22-year-old male, had temporal lobe
epilepsy in the left, language-dominant hemisphere. Pullback
tongue movement was observed upon stimulation of electrode
pair C4 - D4, 1.5 cm inferior to the Sylvian fissure and well
within the superior temporal gyrus. Furthermore, upon stimu­
lation of electrode pair C3 - D3, at 0.3 cm inferior to the Sylvian
fissure, side-to-side tongue movement was arrested (D - 3 in
Fig. 2D). The remaining patient was a 30-year-old wonlan with
complex partial and secondary generalized seizures in the left,
language-dominant hemisphere. Numbness of the tip of tongue
was observed upon stimulation of the electrode pair 1 cm
inferior to the Sylvian fissure-central sulcus junction.
Table 2 (A - C) Distribution of motor, sensory, arrest and mixed responses in patients without organic lesions (A), with
fronto-parietal lesions (B) and with temporal lesions (C)
(A) Patients without organic lesions
Sensory
Motor
5.-------,---------,----r--------.------,---------,
5......------------,-------,-----y-----r-------r-----,
(em)
(em)
20%
9%
14%
33%
12%
41%
13%
6%
27%
6?'6
6%
6%
+4.5(em) +3.0
cs
+1.5
6%
3%
SFL...----------'---------'-----L...---------'------'-------'
-1.5
-3.0
SF
" - - _ - - - L_ _---'--_ _. L . . . - _ - - - - ' ­
+4.5(em) +3.0
-4.5
cs
+1.5
-1.5
-"--_--'
-3.0
-4.5
Mixed
Arrest
5.----,-------,----r--------.-----,-------,
(em)
5......---------,----,.-----y--------r-----.--------,
(em)
14%
10%
10%
3 0/0/
11%
7%
6°0
6 0/0/
13%
10%
30%
11%
5%
4%
5
5%
8%
11%
22%
3%
0
/
/0
SF
SF
+4.5(em) +3.0
+1.5
CS
-1.5
-3.0
-4.5
+4.5(cm) +3.0
+1.5
CS
-1.5
-3.0
-4.5
Sensory-motor cortical tongue representation
125
(B) Patients with fronto-parietal lesions
Motor
Sensory
5
5
1 7%
(CfIl)
33%
(em)
25%
29%
25%
1 7%
33%
17%
13%
20%
17%
SF
25%
SF
+4.5(em) +3.0
cs
+1. 5
-1. 5
-3.0
-4.5
+4.5 (em) +3.0
cs
+1.5
Arrest
-1.5
-3.0
-4.5
Mixed
5.------r-----r-------y-----,----.,.--------,
11%
(CfIl)
25%
(em)
17%
17%
1 7%
20%
2:,%
20%
17%
20%
38%
25%
1 7%
SF
SF
+4.5(em) +3.0
+1. 5
cs
-1.5
-3.0
'---------'--------'---~---'---------'-----------'
+4.5(cm) +3.0
-4.5
cs
+1. 5
-1.5
'-3.0
-4.5
(c) Patients with temporal lesions
Motor
5
(em)
67%
33%
25%
60%
25%
14%
50%
33%
SF
+4.5(cm) +3.0
+1.5
cs
-1.5
-3.0
-4.5
The percentages in each case correspond to the numbers in A -c, respectively. Numbers in each box indicate percentage of responses to
electrode stimulation to all electrode pairs stimulated in the cortical segn1ents. For example, in A, for motor responses, in the particular
cortical segment 1.5 cm anterior to central sulcus and 1- 2 cm superior to Sylvian fissure, 41 % of electrode pairs showed responses (11
electrode pairs out of 27 total). CS = central sulcus; SF = Sylvian fissure.
Parietal motor and frontal sensory responses
For the analysis of paradoxical responses, all patients (with and
without organic lesion) were included (Tables 6 and 7).
Paradoxical nlotor or sensory cortical responses were found in
17 out of 40 patients. In six patients some of the motor responses
were observed in the parietal lobe instead of the frontal lobe.
In seven patients, some of the sensory responses were observed
in the frontal lobe instead of the parietal lobe. They were
reported as discrete tingling or numbness identical with post­
central sensory response (Libet et al., 1964; Libet, 1973;
Amassian et al., 1991; Cohen et al., 1991). In four patients,
both frontal sensory and parietal motor responses were ob­
served. Five of the 12 parietal motor responses were part of
mixed responses. Eight of the 12 frontal sensory responses were
part of mixed responses (Table 6).
Age, sex, duration of illness and cognitive function level in
patients having paradoxical responses were compared with the
same factors in patients without such responses (Table 7). There
126
E. Urasaki et al.
Table 3 (A and B)
(A) Location expressed as distance (in centimetres) from the central sulcus (CS) or Sylvian fissure (SF) of each type of tongue response
in patients without brain lesions compared with patients with lesions. Minus sign at mean value indicates posterior to the central sulcus.
Abbreviations as in Table 1.
Patients
Motor arrest
Motor
Mixed
Sensory
From CS (em)
From SF (em)
From CS
Patients without
organic lesions
0.70 ± 1.21
(n = 19)
2.05 ± 1.0
(n = 19)
0.77 ±0.93* 1.60 ± 0.85** 0.03 ±0.89 1.56 ± 1.0
(n = 48)
(n = 48)
(n = 15)
(n = 15)
Patients with
fronto- parietal
lesions
0.39±0.97
(n = 7)
2.74 ± 1.26
(n = 7)
(n = 10)
From CS
From SF
From CS
From SF
-0.83 ±0.72 1.03 ±0.87
(n = 6)
(n = 6)
0.34 ± 1.30 1. 76 ± 1.33
1.68 ±0.91 * 3.16 ± 1.09** 0.43 ±0.83 1.96 ±0.89
(n = 8)
(n = 5)
(n = 5)
(n = 10)
(n = 8)
0.40± 1.36
(n = 12)
Patients with
temporal lesions
From SF
1.25 ±0.81
12)
(n =
(B) Statistical comparison (t test with Bonferroni's correction) of the cortical locations of each tongue response in patients without
organic lesion. Abbreviations are as in Table 1.
Distance
M versus S
M versus X
S versus X
A versus M
A versus S
From CS
p < 0.001
P < 0.05
NS
NS
P < 0.005
NS
From SF
NS
NS
NS
NS
NS
NS
*p <
0.05~
A versus X
**p <0.001 (t test with Bonferroni's correction for multiple comparisons)
were no statistically significant differences between the two
groups in relation to any of the factors.
Table 4 Comparison of the cortical locations of unilateral
and bilateral tongue responses in patients without organic
lesion
Paradoxical responses in patients with brain lesion
versus responses in patients without brain lesion
Eight of 12 (67 %) patients with brain lesion had paradoxical
responses (Tables 6 and 8). Four patients showed frontal sensory
and two showed parietal motor responses. The remaining two
patients had both parietal motor and frontal sensory responses.
Paradoxical responses were seen in six out of seven patients
with a fronto-parietal lesion (86 %), and two out of five patients
with a temporal lesion (40 %) (Table 8). Of the 28 patients
without brain lesion, nine (32 %) had paradoxical responses.
Thus the brain-lesion group had a higher chance of having
paradoxical responses (P < 0.05), particularly those with
fronto-parietal lesion (P < 0.025) (Table 8). In the patients
with temporal lesions, there was no statistical significance to
the presenting paradoxical responses (P = 0.55).
There were 12 parietal motor responses. Ten of the 12
responses were localized in the first 1.5 em posterior to the
central sulcus, and the remaining two responses were located
within 3 em posterior to the central sulcus. Eight of 12 frontal
sensory responses were within 1.5 em anterior to the central
sulcus, and three responses were within 3 em anterior to the
central sulcus (Table 6).
Discussion
Tongue representations on the corlex
Our study indicated that the cortical tongue area extended
beyond the line 1.5 em anterior to the central sulcus and also
From central sulcus
From Sylvian fissure
From central sulcus
From Sylvian fissure
Bilateral M
IT nilateral M
(n = 32)
(n = 16)
0.85 ±0.93
1.63 ±0.87
0.59±0.97
1.54 ±0.80
NS
NS
Bilateral S
Unilateral S
t
(n = 4)
(n = 2)
-1.08 ±0.49
0.90±0.88
-0.35 ±0.85
1.30 ± 0.80
t test
test
NS
NS
Bilateral M = bilateral motor responses, pulling back of the
tongue without laterality ~ unilateral M = unilateral motor
responses, lateral tongue deviation~ bilateral S = bilateral sensory
responses, bilateral tongue sensation~ unilateral S = unilateral
sensory response, unilateral tongue sensation contralateral to the
side of stimulation~ minus sign at nlean value indicates posterior
to the central sulcus.
extended posterior to the central sulcus (Tables 1 and 2 and
Figs 1- 3). The mean distance of the pre- and postcentral sulcus
from the central sulcus is known to be -- 10- 12 mm (Ono
et al., 1990).
The tongue area showed a wide distribution in patients without
organic lesions (Tables 1 and 2, Figs 1 and 2) and this
distribution was wider still in patients with evidence of an
organic lesion. It must be noted that, in the patients without
fronto-parietal lesions, the grid rarely covered the area 3 em
away from the Sylvian fissure. Nonetheless, tongue responses
Sensory-motor cortical tongue representation
127
Table 5 (A and B) Statistical comparison of tongue responses by type, in frontal region
versus parietal region (A), and comparison of response rates, by location, in motor responses
versus sensory responses (B)
(A)
Total response
(A+M+X+S)
Motor arrest
(A)
Motor
(M)
Mixed
(X)
Sensory
(S)
Response rates %
in frontal versus
parietal
23.7
18.9
4.7
4.7
15.4
6.1
3.2
4.7
0.4
3.4
x2
NS
NS
P < 0.01
NS
P < 0.05*
test or Fisher's
exact test
(B)
Motor versus sensory McNemar's test
Whole area
Frontal
Parietal
P < 0.001
P < 0.001
NS
Note that McNemar's test is applied to B, because the rates of occurrence of motor and sensory are
compared with each other in the same area, such as frontal, parietal and whole (frontal and parietal)
areas. *Fisher's exact test is only used for sensory response because the data contain a number
below 5.
Table 6 (A and B) Summary of the patients with paradoxical frontal sensory and parietal
Inotor responses
(A)
No. of patients
Patients with
organic lesions
Frontal sensory response
alone (FS)
Parietal motor response
alone (PM)
7
1
2
1
6
Angioma*
Astrocytoma***
Cortical dysplasia
(frontal)
Patients without
organic lesions
3
Both FS and PM
Angioma**
Astrocytoma t
4
1
1
Post-resection of
2
temporal astrocytoma
4
2
(B)
Frontal sensory response
No. of responses
Only sensory response
Part of mixed response
Total
Location of responses
Parietal nlotor response
4
8
Only motor response
Part of mixed response
12
From central sulcus
0- 1.5 cnl
1.5 -3.0 cm
8
4
7
5
12
From central sulcus
about -1.5 cm
-1.5 to about - 3.0 cm
o to
10
2
Note that A is nunlber of patients, B is number of responses. One patient could have more than one
response. *Patient had 1.5 x 2 cm angioma. The lesion was located in prefrontal subcortex; **in this
patient the size of angioma was 0.5 x 1 cm and it was located in the prefrontal cortex; ***in these two
patients, the size and location of the lesions were 3 x 2.5 cm in the precentral area and 4 x 4 cm in the
pericentral area, respectively, seen on MRI; tin this patient, a 4 x 3.5 em lesion was found in the
prefrontal area on MR!. Histological study showed low-grade astrocytoma.
were often obtained at the distal edge of the grid (see Fig. 2),
iInplying that tongue responses could occur even more superior
to the Sylvian fissure in these patients. Furthermore, even in
the group with small frontal lesions without mass effect, tongue
responses anterior to the line 1.5 cm from the central sulcus
were frequently found (see D6 in Fig. 3A), a finding suggesting
128
E. Urasaki et al.
Table 7 Statistical cornparisons of clinical factors benveen the patients with and without
paradoxical responses
Patients with paradoxical
responses
Patients without paradoxical
responses
Age (years)
Duration of seizure
(years)
24.7 ± 11.7 (n
14.7 ± 11.8 (n
25.8±9.4 (n = 23)
14.2 ± 9.0 (n = 23)
NS
NS
VIQ
PIQ
Total IQ
Word tl uency score
86.4 ± 11.8 (n
10)
85.2 ± 9.5 (n = 10)
88.2±15.3 (n = 11)
9.4±3.0 (n = 8)
87.1±16.2 (n
17)
83.8 ± 10.3 (n
17)
83.6± 13.6 (n
17)
11.0 ± 2.6 (n = 15)
NS
NS
NS
NS
t
17)
17)
test
x2
Male/female
13/10
9/8
test
NS
VIQ, PIQ = verbal and perfornlance intelligent quotients.
Table 8 Paradoxical responses in patients with and
~vithout
brain lesion
Negative MRI for
brain lesion (N)
Brain lesion fronto-parietal
or temporal areas (FPT)
Brain lesion limited to
fronto-parietal area (FP)
Brain lesion limited to
temporal area (T)
Patients with/without
paradoxical responses
With: 9
Without: 19
8
4
6
1
2
3
Rate (percentage) of
paradoxical responses
32%
(9/28)
67%
(8/12)
86%
(6/7)
40%
(2/5)
On statistical conlparison (Fisher's exact test) of the groups of patients, the occurrence of responses was significantly greater in all
patients with lesions (FPT) (P = 0.047 < 0.05) and in patients with fronto-parietal lesions (FP) (P = 0.016 < 0.025) than in patients
with no evidence of brain lesions (N). There was no significant difference between patients without lesions (N) and those with temporal
lesions (T) (P = 0.05).
that dislocation or displacement of the 'primary' tongue area
by pericentral lesion is not simply a factor of far anterior
displacement of the tongue area by a mass or space-occupying
lesion. This concept was also supported by the findings in
patients without organic lesion, who showed wide distribution
of the tongue area in an antero-posterior direction (Tables 1
and 2).
Penfield and Boldrey (1937), Penfield and Rasmussen (1950),
Libet et al. (1964), and Picard and Olivier (1983) have not
observed such a wide distribution of tongue motor responses,
except in one case of infiltrative glioma reported by Penfield
and Boldrey (1937). Comparisons between their findings and
ours are difficulC because their reports do not give specific
details about their patients, including whether or not they had
organic lesions (Penfield and Boldrey, 1937 ~ Penfield and
Rasmussen, 1950~ Picard and Olivier, 1983). However, sensory
tongue response occurring with stimulation outside the Rolandic
region was reported by Penfield and Boldrey (1937). In
addition, stimulation of the superior tenlporal gyrus elicited two
tongue sensory responses: one at the tip and one contralateral
to the side of cortical stinlulation (Penfield and Boldrey, 1937).
Our study is in accord with their report.
The issue of current spread is always difficult to resolve in
cases of surface stimulation of human cortex, whether it occurs
intra- or extra-operatively (Penfield and Boldrey, 1937 ~ Penfield
and Rasmussen, 1950~ Picard and Olivier, 1983 ~ Uematsu et
al., 1992a), and it could be the reason for the apparent wide
distribution of the cortical tongue area. It is, however, unlikely
that all our results could be accounted for by current spread.
If current spread affects the area adjacent to the stimulated
electrodes, direct stimulation of the area would be expected to
elicit similar tongue responses. However, we frequently
observed a non-tongue-response area between the areas where
apparent tongue responses were elicited (Fig. 2B and D). This
indicates that current spread is not the sole explanation for the
wide distribution.
It is already known that particular body parts (e. g. finger,
hand or head or face) may have nlultiple representation on the
cortex, e.g. in the first somatosensory area (SmI) or first
somatomotor area (MsI) (Dreyer et al., 1975 ~ Strick and
Preston, 1979). Although it was described in studies using a
finer micro unit recording (Dreyer et al., 1975~ Strick and
Preston, 1979), this concept may also be applied to our
observations obtained with grid brain mapping. These obser­
vations are supported by similar brain-mapping studies carried
out by others (Murphy and Gellhorn, 1945).
Sensory-motor cortical tongue representation
Low rate of sensory response
Sensory responses were less frequent than motor responses even
in the postcentral region (Table 5). It is unlikely that this is due
entirely to different levels of excitability between the cortical
area anterior to the central sulcus and the cortical area posterior
to the central sulcus, because there was no difference in the
rate for total tongue responses between these sites (Table 5).
In our assessments, we slowly increase the intensity of the
stimulus at each site until the appearance of a response or until
we reach the 15 rnA Iimit of our machines (Lesser et al., 1987 ~
Uen1atsu et al., 1992a), which optimizes the chance of detect­
ing functional changes. Libet et al. (1964) and Libet (1973)
en1phasized that the electrical threshold for postcentral motor
response was higher than that for postcentral sensory or
precentral motor response. However, the present study showed
that over half (58 %) of the parietal motor responses were
detected without conscious sensation (Table 6).
One of the reasons for the low rate of sensory response might
be that the disc electrodes mainly stimulated the surface of
exposed cortical sensory area 2 and part of area 1, but less of
area 3, because it is buried deep in the posterior wall of the
central sulcus (Williams et al., 1989). Current spread was
n1easured to be about one-quarter of the original value when
the recording site was 2 mm away from the stimulation site
(Murphy and Gellhorn, 1945) and the mean depth of the central
sulcus was -- 16 n1n1 (Ono et al., 1990) so that current intensity
in areas 3 A and B should be nluch lower than that at the surface
and would likely be subthreshold for producing functional
changes.
Compared with area 3, areas 1 and 2 are similar to association
cortex both morphologically and physiologically (Iwamura,
1991). Area 3 contains nunlerous granular cells, which are
particularly associated with afferent projections, while areas 1
and 2 have increased numbers of pyramidal cells, which are
involved in information transmission (Williams et al., 1989 ~
Iwamura, 1991). Single neuron studies disclosed an increased
number of movetTIent-related neurons in areas 1 and 2 (Schwarz
and Fredrickson, 1971: Iwamura, 1991). Iwamura (1991) stated
that in area 2 of the tTIonkey, 10.6 % of neurons fired only upon
active movement and 31.3 % showed no clear receptive fields,
while only 56.6% fired upon superficial and deep sensation.
These results support our finding of relatively few sensory
responses evoked by stimulation of the surface area of the
postcentral gyrus.
The differences in test conditions between our study and
previous reports must also be considered. Many of the previous
stimulation-based studies of functional- anatomical relationships
in the hUITIan brain mapping have been carried out intra­
operatively (Cushing, 1909~ Foerster. 1936b~ Penfield and
Boldrey, 1937: Penfield and Rasmussen, 1950~ Walshe, 1951~
Libet et al., 1964: Goldring and Ratcheson, 1972 ~ Libet, 1973 ~
Celesia et al., 1979: Woolsey, 1979~ Picard and Olivier, 1983).
Obviously, intra-operative conditions include local anaesthesia,
possibly with light sedatives or narcoticentral sulcus, all of
which could influence cortical responsivity.
129
Mechanism of frontal sensory and parietal motor
response
Paradoxical response
Debate continues concerning parietal motor and frontal sensory
responses (Foerster, 1936a, b ~ Penfield and Boldrey, 1937 ~
Penfield and Rasmussen, 1950~ Libet et al., 1964~ Libet,
1973). Recently, Baumgartner et al. (1992) also noted these
paradoxical responses in their study using a subdural grid.
According to Libet et al. (1964) and Libet (1973), parietal
motor responses were described as non-smooth, intermittent
moven1ents in comparison with 'pyramidal type' movements
from the frontal lobe. In our study it was difficult to distinguish
these characterists in tongue motor responses. Libet et al. (1964)
and Libet (1973) stated that no frontal sensory response could
be elicited in portions of the brain which were not specifically
epileptogenic, except for motion sensation accompanying
movenlents. In the present study, paradoxical responses
occurred in eight out of 12 patients with and nine out of 28
patients without organic lesions (Table 6). A recent study using
magnetic coil stimulation detected a frontal sensory response
(tingling) in a minority of normal subjects (Amassian et al.,
1991). Both the Amassian et al. study and our own suggest that
the normal brain has the potential for paradoxical responses.
Cortico-cortical connections
In a cortical stimulation study, it is almost impossible to
determine whether the responses result from the stimulated sites
or from cortico-cortical or cortico-subcortical connections,
including thalamus and more caudal nuclei (Williams et al.,
1989).
Areas 1 and 2 have bidirectional projections to areas 4 and
6, and reciprocal fibre connections exist between areas 1, 2,
5 and 7. In contrast, area 3b has only unidirectional connections
to areas 1 and 2 (Jones and Powell, 1969~ Pandya and Kuypers,
1969: Yamaguchi and Knight, 1990). Thus stimulation of areas
4 and 6 could activate areas 1 and 2 and vice versa. The present
study showed that 67 % of frontal sensory responses were
expressed as part of a nnxed response, which could be the result
of these cortico-cortical connections. It should be noted,
however, that cortico-cortical connections are not the sole factor
in frontal sensory or parietal motor responses, because, as
reported by Penfield and Rasmussen (1950), these responses
still could be elicited after excision of the postcentral gyrus or
precentral gyrus, respectively (Brodmann's areas 4 and 6 and
areas 3, 1 and 2).
As noted above, tongue representation extended beyond the
precentral and postcentral gyri, perhaps therefore including
areas 44 and 45, and areas 43 and 40. Efferents from areas
44 and 45 are shown to terminate in area 4 (Zilles, 1990). It
is possible that area 40 and its adjacent area 43 in the parietal
lobe also are connected to the inferior frontal gyrus, including
areas 44 and 45.
Our data are in good agreement with the theory that
physiologically, parts of areas 8, 44 and 45, together with
130
E. Urasaki et al.
area 6, are in the premotor area, and that the whole precentral
area, including area 4, belongs in the first somatomotor area
(Williams et al., 1989), although the cyto-architecture of
Brodmann differentiates them (Williams et al., 1989; Zilles,
1990). Brodmann's map and numeration are widely used
as a reference for cortical locations, but recent pigmento­
architectonic observations of the cortex indicate the difficulty
of dividing areas 43 and 40 from areas 3, 1 and 2 at the level
of the tongue area, because they can be included in a parietal
magnopyramidal region (Zilles, 1990).
Other physio-anatomical supports
Sensory cells were found in motor cortex by single neuron
studies (Goldring and Ratcheson, 1972; Asanuma et al., 1979).
Areas 3, 1 and 2 also contribute motor (pyramidal) fibres in
monkey and man, and some (a minority) are generated from
temporal and even occipital lobes in cats (Walberg and Brodal,
1953; Williams et al., 1989). These findings might explain
in part the paradoxical frontal sensory and parietal motor
responses, as well as the motor responses obtained in the
temporal lobe.
Second sornatosensory area (SmII)
The anterior part of area 40 and the caudal part of the
perirolandic area comprise the region where the second
somatosensory area (SmII) son1etimes appears (Penfield and
Rasmussen, 1950; Celesia, 1979; Williams et al., 1989).
Penfield and Rasmussen (1950) were able to identify SmII in
both prerolandic and postrolandic areas adjacent to the Sylvian
fissure. The SmII is predominant!y sensory but motor function
has also been documented in this area (Penfield and Rasmussen,
1950; Williams et al., 1989). Therefore, some parietal motor
responses might be evoked through activation of efferent
pathways originating in SmII (Celesia, 1979; Luders et al.,
1985; Williams et al., 1989), some frontal sensory responses
might be activated by stimulation of cells receiving afferents
from ventrobasal or posterior nucleus of the thalamus (Celesia,
1979; Luders et al., 1985; Williams et al., 1989) and para­
doxical responses might be evoked via cortico-cortical connec­
tions between SmII and SmI or MsI (Pandya and Kuypers,
1969).
However, SmII is known to represent mainly the extremities,
and it is usually buried in the Sylvian fissure. The latter fact
explains the low appearance rate of SmII; it was shown in only
10 out of over 400 patients on cortical stimulation study by
Penfield and Rasmussen (1950) and only one out of over 50
patients in the somatosensory evoked potential study of Luders
et al. (1985). Therefore, the paradoxical responses seen in 17
cases in this study seen1 unlikely to be explained by stimulation
of SmII.
with drug injection in the brain (Alloway et al., 1989) and
with the strength of cortical stimulation (Liddell and Phillips,
1950; Cure and Rasmussen, 1954) in both animals and
humans-findings all indicating plasticity of brain (Green and
Walker, 1938; Glees and Cole, 1950). These phenomena are
considered to result from unmasking of existing but ordinarily
silent connections or sprouting of new synaptic contacts
(Merzenich et al., 1983a,b; Alloway et al., 1989; Cohen et al.,
1991; Iwamura, 1991). Similar mechanisms also might explain
some of the paradoxical responses in our study, perhaps
activated by epilepsy or organic lesions. All of these data
strongly suggest that brain is not constructed of •static mosaics'
with invariable relationships to one another.
Conclusion
As indicated by the present study, paradoxical responses, such
as frontal sensory and parietal motor responses, are relatively
common findings upon stimulation of the cortical tongue area
in patients with epilepsy. The surgeon should be aware of the
existence of such paradoxical responses, particularly during
cortical stimulation, to establish the junction of the central sulcus
and Sylvian fissure, especially in cases with fronto-parietal
lesions. The anatomist and physiologist should be aware of them
when attempting to determine the overall anatomical - functional
relationships of human cortex.
Acknowledgements
We wish to thank Mary Bare and Pamela Schwerdt for their
technical assistance in the cortical stimulation study, Robert S.
Fisher, Gregory L. Krauss, Eileen P. Vining and Robert W.
Webber for their valuable assistance, and Sakae Yamamoto,
Associate Professor, Department of Management Science.
Dokkyo University, and Shinya Matsuda, Assistant Professor.
Department of Public Hygiene, University of Occupational and
Environn1ental Health, for their assistance with the statistical
analyses. This study was supported by the Tanaka Memorial
Scholarship Fund provided by his widow Mary Lorenc Tanaka,
and by grants fron1 the National Institute of Deafness and other
Conm1unicative Disorders R03-DCO 1181), The National
Institute of Neurological Disorders and Stroke (RO l-l'JS26553),
the Seaver Foundation, the Whittier Foundation and the
McDonnell-Pew Program in Cognitive Neuroscience.
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Received August 18, 1992. Revised July 14, 1993.
Accepted September 11, 1993