neurofpeport

WE present the case of a patient with a lesion of the thala-
mus who was completely anaesthetized on his right side.
He was unable to detect and describe a tactile stimulus
applied to his affected right arm, but could direct his nor-
mal left hand toward the specific right hand site where the
stimulus had been applied when so instructed (‘blind
touch’). Strikingly, this pointing ability disappeared when
the patient had to indicate on a picture of an arm where
the stimulus was applied, and when he had to name the
stimulus location during his pointing. Similar results were
also obtained for localizing the unfelt fingertip (‘blind pro-
prioception’). Neuropsychological case studies have dem-
onstrated that brain lesions can produce reciprocal
dissociations between object identification (what is the
object) and object-oriented action (how to direct a move-
ment to the object). Along these lines, it is suggested that
our patient exhibited a dissociation between a ‘where’
system and a ‘how’ system for tactile and proprioceptive
stimuli.

Key words: Touch; Proprioception; Implicit perception;
Blind touch; Action; Perception; Representation; Sensori-
motor; Consciousness; Neuropsychology

Cognitive Neuroscience and Neuropsychology

NeuroReport 6, 506-510 (1995)

Implicit processing of
somaesthetic information:
a dissociation between
where and how?

Yves Rossetti," Gilles Rode’?
and Dominique Boisson?

Wision et Motricité, INSERM U94, 16 avenue
doyen Lépine, 69500 Bron; Hopital Henry
Gabrielle, Hospices Civils de Lyon, B.P. 57,
69565 Saint-Genis Laval cedex, France

CA Corresponding Author

Introduction

Implicit processing of somatic sensation following a
lesion of central somatosensory areas has been
reported by several authors.'* Typically, these patients
could point to a location stimulated on their ‘deaffer-
ented’ forearm while unable to report any tactile ex-
perience: this phenomenon has been considered as a
tactile equivalent of blindsight. These ‘blind touch’
observations have raised several questions. First, it has
been stressed that a significant influence of stimulus
location on pointing responses occurs despite the lack
of conscious report about the stimulus applied. It can
be argued however that the pointing performance
obtained in such patients might be observed with other
kinds of forced-choice responses, e.g. verbal. Indeed, it
has been shown in normal subjects that verbal response
about localization can be more accurate than verbal
report about detection of the same stimulus.‘ In a case
reported by Brochier et al,> significant performance
was observed in a verbal forced choice task, but no
pointing task was presented to the same patient. Com-
parison of verbal and motor forced choice responses in
the same patient would therefore be of great interest.
Second, if one wishes to interpret this phenomenon in
terms of a dissociation between different streams of
information processing such as ‘what’ and ‘where’,?°
one needs to demonstrate a dissociation not only be-
tween different modes of response, but also between
similar responses when sustained by different process-

A preliminary report about this work was presented at the Inter-
national Congress of Stroke Rehabilitation, Berlin 1993.

506 Vol 6 No3 15 February 1995

ing, ¢.g. pointing movements sustained either by a
where or by a how processing. Several anatomical
interpretations of so-called blind touch have been pro-
posed. In the case reported by Paillard et a/,? with a par-
ictal lesion, spared frontal somatosensory evoked
potentials (SEPs) implied a possible involvement of
precentral areas. The patient described by Brochier et
al® had an anterior parietal lesion, frontal SEPs were
not reported and the interpretation focused on the
potential role of the posterior parietal cortex. Another
possible hypothesis is that uncrossed somatosensory
projections (revealed by infantile lesions*”) can provide
unconscious information to the healthy limb pointing
at the affected limb.

We had the opportunity to study a patient (J.A.) who
presented with a complete sensory loss of the right half
of the body.® This case allowed us to compare verbal
and pointing responses using the same forced choice
paradigm, and to compare pointing made in direct res-
ponse to the stimulus or after a representation of the
stimulus location was constructed. In addition,
detailed paraclinical investigations (SEPs, PET)
allowed discussion of the above-mentioned anatomical
hypotheses.

Previous neuropsychological reports have focused
on the dissociation between different pathways per-
taining to the same modality. However, in the visual
system, interconnections have been described between
the dorsal and the ventral streams.®° This anatomical
feature could supply a basis for a functional interaction
between so-called parallel systems. This assumption
was tested for touch and proprioception by asking J.A.
to produce two forced choice responses (pointing and
verbal) simultaneously.

© Rapid Communications of Oxford Ltd
Blind touch and blind proprioception

neurodpeport

Material and Methods

Case report: J.A. was a 64-year-old ambidextrous male
who developed a sudden right hemiparesia with a com-
plete sensory loss in the right half of the body follow-
ing a cerebral haemorrhage within the deep territory of
the sylvian artery. Clinical examination showed a
Dejerine-Roussy syndrome with right incomplete
hemiplegia, complete hemianaesthesia of the right
body and ipsilateral choreo-athetosic movements.
Four months later, J.A. would not use his right arm
spontaneously. He could nevertheless reach and
manipulate objects under visual control. Without
vision, alterations of the movements were comparable
with those of a centrally deafferented patient described
by Jeannerod et a/'' (see also Ref. 2). In contrast with
this latter case, the tactile and proprioceptive deficit
was complete, even in the right facial territory, sensi-
tivity to temperature, pain, vibration, deep pressure
and passive movement being abolished. Identification
and detection of all objective somaesthetic stimuli, ste-
reognosic recognition and matching were impossible
on the right side. J.A. spontaneously reported an
illusory sensation of his right arm moving when he was
lying in the dark. He showed no impairment of mem-
ory, language, gnosic or praxic abilities and he could
name, detect, match loci and objects on his left side
normally. No visual field defect or visual extinction
was noted.

MRI inspection showed a lesion of the left ventrolat-
eral and ventroposterolateral nuclei of the thalamus
(Fig. 1). Recording of somatosensory evoked poten-
tials showed a complete absence of the parietal (post-
central) response (N20-P27-P45 components) and the
frontal (precentral) response (P22-N30) following
electrical stimulation of the second and third digits of
the right hand. An attempt to record ipsilateral res-
ponses failed to show any significant signal. A PET
study (Ref. 9, FDG) showed hypometabolism in the
lesioned subcortical area and in the whole left parietal
and frontal cortex, consistent with a thalamocortical
diaschisis (see Ref. 12). Vibratory stimulation of the
right hand elicited no activation of the left thalamus nor
the left somatosensory areas. These data support a sev-
ere left hemisphere deafferentation following an ipsi-
lateral thalamic stroke.

Procedure: To test the patient’s tactile ability, stimuli
were delivered to his right forearm and hand with the
tip of a pencil, left in place until the patient initiated his
response. The investigator randomly stimulated loca-
tions that had been demonstrated on the left normal
arm prior to the session. Since the patient did not feel
the stimuli applied, he had to be instructed when to
produce his response. No information was provided to
the patient about his performance during the experi-
ment. However, given the lack of explicit localization
information, the patient required considerable encour-

agement. The first experiment investigated J.A.’s abil-
ity to locate tactile stimuli applied to his right hand.
The patient was blindfolded and motor and verbal per-
formances were compared. Motor responses involved
pointing movements using the left index finger. No
constraint was imposed on movement speed, but the
patient was encouraged not to delay his response, since
preliminary experiments have shown that long laten-
cies decrease performance. Pointing movements were
recorded by a video camera. Verbal responses were
obtained by a forced-choice paradigm among the six
possible stimulus locations demonstrated previously.
In order to test whether the somatic sensation was pro-
cessed only for motor interaction with the stimulus or
whether it had also a value for proper location percep-
tion, we used another pointing response which was not
directed to the stimulus. In this second experiment, a
drawing of an arm (scale 1) was placed on the table 20
cm left of his hidden, stimulated right arm. J.A. was
then asked to point on the drawing to the point match-
ing the location of the stimulus applied to the arm. In
the third experiment, the possible interference between
the systems responsible for the pointing and the verbal
responses was investigated. J.A. was required to prod-
uce simultaneously the pointing movement and the
verbal response to a single tactile stimulus.

When testing proprioceptive information process-
ing, J.A. was blindfolded. A tablet was used above
which the patient’s right fingertip was positioned. The
right, affected arm was manipulated by the investigator
in sucha way so as to place the right fingertip on one of
two locations, 30 cm in front from the patient’s trunk
and 10 cm respectively to the left and right of his sagit-
tal axis. In order to avoid interference between tactile
and proprioceptive information processing, the arm
was provided with as little tactile information as poss-
ible and was manipulated by touching areas as close to
fingertip as possible. Since no conscious processing of
arm proprioception was available to J.A., two guessing
responses were evaluated. In one session, he was asked
to point underneath the tablet to the point correspond-
ing to the location of his right index fingertip. In
another session, J.A. was asked to guess verbally
whether his fingertip was on the right or on the left
location. In the final session, J.A. was asked to produce
simultaneously the verbal and pointing responses for
each trial.

Performance: Performance was evaluated by two
means. First, analysis of verbal responses and compari-
son between verbal and pointing responses used a
dichotomous measurement (correct vs incorrect). We
assigned the value of one or zero to each trial, respect-
ively for correct and incorrect responses, i.e. inside vs
outside the stimulated territory (e.g. the whole finger
in the case of fingertip stimulation). Second, for com-
parison between pointing conditions we also used a
quantitative measurement of the distance between

Vol 6 No 315 February 1995 507
neuro¢peport

Y. Rossetti, G. Rode and D. Boisson

FIG. 1, Axial T1-weighted MRI images show a hypo-intensity limited to
the ventrolateral and the ventroposterolateral thalamic nuclei and
extending into the posterior part of the thalamoparietal projection of
the left hemisphere. The cortical areas and the right hemisphere were
intact.

stimulus location and pointing. For this purpose, per-
formance was measured as the distance from stimulus
location to the actual point reached on the arm when
pointing directly on the arm, and as the distance from
the point on the drawing corresponding to the actual
stimulus position to the actual hand pointing on the
drawing when pointing on the arm drawing. One value
was attributed to each trial and the means and s.e.m.
over trials were computed for each condition. Similar
dichotomous and distance measurements were calcu-
lated for the proprioceptive task. Since the two possible
fingertip locations were aligned on a frontal axis, the
distance between the target fingertip and the pointing
location was measured along the same direction.

Statistics: Two statistical methods were used to analyse
the performance measures used. Chance performance
for the dichotomous guesses was evaluated by testing
departure of the observed distribution from the law of
Laplace-Gauss'. Comparison between two pointing
conditions was based on the distance measurements.
The mean distances obtained in two conditions were
compared by one way ANOVA.

Results

Touch: During the pointing sessions, J.A. repeatedly
performed above chance level (Fig. 2). In the first
experiment using six stimulus locations on the hand,

508 Vol 6 No 3 15 February 1995

ON ARM

ON DRAWING

FIG. 2. {A} Points reached when J.A. pointed to tactile stimuli applied to
six loci of the right hand (anterior ungual phalanx of the five fingers +
the palm centre). Arrows indicate stimulus location, from which a line
was drawn to each trial point reached by J.A. Black dots indicate correct
reaches. (B) Same conventions as in A. A set of eight stimulus locations
was used in the second experiment: the posterior ungual phalanx of the
five fingers + the palm centre + the wrist + the middle forearm. Pointing
with the left index finger was made toward the locus stimulated (1)
directly on the right forearm (2) on an arm drawing of the right forearm
(scale 1).

J.A. reached the stimulated area in 18 out of 40 trials,
which was significantly above the chance level of 5/40
(p < 0.001). The errors observed exhibited the same
directional bias as in the case reported by Paillard et
al,” i.e. toward the palm. Contrasting with the pointing
responses, verbal performance (4/21, p > 0.10) was
never significantly different from chance.

In an experiment using eight possible stimulus loca-
tions on the right forearm, J.A. provided 17 correct res-
ponses out of 40 trials (p < 0.001). With the same
stimulus set, but when pointing on the arm drawing,
J.A. provided only six correct responses (NS). In
addition, the mean distance ( + s.e.m.) between the
stimulus and the response increased from 8.7 + 0.96
cm to 12.3 + 1.20 cm. This difference attained statisti-
cal significance (F(1,79) = 5.57; p < 0.025). This sug-
gests that J.A.’s ability to produce a significant
performance is restricted to movements directly aimed
at the stimulus itself but does not apply to similar
movements matching stimulus location on a picture.

When J.A. was required to produce the two res-
ponses at the same time, there was a coincidence be-
tween the pointing and the verbal responses. However,
Blind touch and blind proprioception

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FAG. 3. (A) Pointing error (mean distance + s.e.) between the stimulus
and the point reached by J.A.) in the pure condition (‘pointing’) and
when J.A. had to identify verbally the locus stimulated (e.g. index or
palm) during his pointing movement (pointing + verbal). The pointing
error was significantly larger in the pointing + verbal condition than in
the pointing condition, and not significantly different from that of the
pointing on drawing conditions. (B} Mean frontal positions reached by
left index finger when pointing under the table toward the right index
finger (target finger) positioned either on a left or a right locus. In the
pointing + verbal condition, J.A. was asked to verbalize the side of the
target finger (right vsleft) during the course of the reaching movement,
and the discrimination was no longer observed.

J.A.’s responses were not significantly influenced by
stimulus location (correct trials: 6/40). In addition, the
distance between the stimulus and the response
(12.1 + 1.3 cm) increased to values similar to those
obtained when pointing on the arm drawing (Fig. 3).

Proprioception: When asked to locate his index finger
by pointing with the left hand, J.A. was significantly
influenced by the right finger locus (Fig. 3B). The mean
position reached while the right fingertip was pos-
itioned on the right location was 15.3 + 9.9 cm to the
right of sagittal axis, but it was only 7.4 + 11.3 cm to
the right when the fingertip was positioned on the left
location. Although there was a great variability in the
pointing responses, this difference reached statistical
significance (F(1,39) = 5.55, p < 0.025). The dichot-
omous analysis also showed a significant performance
(29/40, p < 0.05). By contrast, the distribution of ver-
bal forced-choice responses were not significantly dif-
ferent from a random distribution (24/40, p > 0.10).
When the verbal and the pointing responses were pro-

neurofgeport

duced simultaneously, they always were congruent,
but the pointing performance was reduced to random
(17/40, p > 0.10). This was confirmed by the mean
locations reached for the two locations explored, the
mean pointing toward the left location being located
right of the mean pointing to the right location
(1.9 + 18.6 cm to the left vs 4 + 22.7 cm to the left;
F(1,39) = 0.10; NS; see Fig. 3B). As for touch, acti-
vation of a semantic representation of where the target
finger was (required for the verbal response) disrupted
J.A.’s ability to point to this finger. No facilitation of
the verbal response by the simultaneous pointing
movement was observed.

Discussion

A dissociation between pointing and verbal report
has already been reported by Paillard et al? in the case
of a patient with a parietal lesion involving the somato-
sensory area. These authors interpreted this finding in
terms of the classical distinction between the identifi-
cation (‘what’) and localization (‘where’) systems, i.e.
the patient was able to localize the stimulus without
being able to identify it. However, they did not investi-
gate verbal report in a forced-choice paradigm, and
therefore their results could also be explained as covert
information processing that can be observed only
when guessing (through verbal or pointing responses).
In the present experiment, the absence of significant
performance in the verbal forced-choice for stimulus
location demonstrates that tactile information is pro-
cessed not only implicitly but also specifically for
motor purpose. Therefore the present result can be
interpreted as a dissociation between a pragmatic
system responsible for the stimulus driven pointing
and a semantic system responsible for verbally depict-
ing the same stimulus location. A similar kind of dis-
sociation has been previously proposed between a
‘what’ system, responsible for semantic processing,
and a ‘how’ system, responsible for pragmatic process-
ing.” By contrast, the dissociation observed in the
present case holds for stimulus location (i.e. where vs
how) instead of stimulus intrinsic qualities (ic. what vs
how), and can be described for both tactile and pro-
prioceptive stimuli. This dissociation fits with the
more general description of sensorimotor and rep-
resentational modes of spatial information processing
that would respectively use a body-centred and an
environmental frame of reference (see Ref. 20). Vir-
tually all metric qualities of objects in space could be
affected by such a dissociation.

This hypothesis is strengthened by the results
obtained whenJ.A. pointed on the arm drawing. In this
case, he had to produce the same pointing movement,
but combined with a more elaborate representation of
where the stimulus was applied, and consequently his
performance was reduced to chance level. The dis-
sociation observed here would therefore not result

Vol 6 No 3 15 February 1995 509
neurofpeport

Y. Rossetti, G. Rode and D. Boisson

from the difference in the response provided (pointing
vs verbal), but from the difference between the rep-
resentations underlying the responses (how vs where).
Following Paillard,?°J.A. appears unable to process the
tactile information at levels higher than a direct sen-
sorimotor system, i.e. at more symbolic levels. Indeed,
naming the stimulated area requires an underlying rep-
resentation of the stimulus that is more elaborate than
the representation used to point to this stimulus.
Therefore, it can be argued that J.A. is able to point to
the locus of the stimulus (how) without building a rep-
resentation (explicitly or implicitly) of where it is
located.

When the pointing and the verbal responses were
produced simultaneously for either tactile or proprio-
ceptive targets, the pointing performance was reduced
to random. These results confirm that attempts to
elaborate a semantic representation of the stimulus
location can have detrimental effects on the relatively
intact sensorimotor processing. It is important to
notice, however, that no decrease in accuracy (but
rather an improvement) was observed when normal
subjects gave two verbal and motor responses to a
single coloured stimulus.”

Given the qualitative hypoactivation of the left
hemisphere observed in J.A.’s activation study, a poss-
ible substratum for the residual processing observed
here would be the ipsilateral somatic pathways that

account for sensitivity in hemispherectomized
patients.
Conclusion

This observation provides a new illustration of the
relative independence between perception and action
processes. Proprioception and touch can thus reveal a
similar dissociation to that already observed in patients
with optic ataxia or blindsight or after temporal
lesions, ie. when individuals cannot consciously
recognize visual objects (what) but remain able to real-
ize object oriented actions (how) (see Refs 14, 15,
17-19, 22 and 23). In the case of J.A., the dissociation

was observed between perceived stimulus location
(where) and object oriented action (how). Further-
more, the dissociation between these two systems also
showed detrimental effects of verbalization on the
pointing performance. This study suggests that the
processing of tactile stimuli location may involve dif-
ferent brain pathways, depending upon the level of
representation that is activated to produce the res-
ponse, and that conscious processing (e.g. subserving
verbal response) can hierarchically dominate implicit
sensorimotor processing (e.g. subserving pointing).

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ACKNOWLEDGEMENTS: The authors wish to thank Peter Halligan, Marc Jean-
nerod, Kenneth Knoblauch, Denis Pélisson, Marie-Thérése Perenin and Claude Pra-
blanc for their comments on an earlier version of the manuscript. This work was
supported by a grant from Fédération des Aveugles de France to Y.R.

Received 17 November 1994;
accepted 8 December 1994

General Summary

We report here evidence of a striking implicit sensitivity in a patient clinically rendered hemianaesthetic as a result of stroke. This patient
was unable to detect any tactile stimulus applied to his right arm (light touch, deep pressure, movement, heat, cold, pinch, pain), but
remained able to point with his healthy left arm at the locus stimulated. By contrast, he failed to guess verbally the locus of the stimulus. In
addition, he was unable to demonstrate stimulus location on an arm picture by poi
about the right arm was available to left hand movement interacting with the stimulus, but could not be accessed by mental representation.
Two dissociated systems are proposed account for this phenomenon: a ‘how’ system, responsible for directing action to the stimulus, and
a ‘where’ system, responsible for representing stimulus location. In search for a possible interaction between these two systems, our
patient was required to produce the pointing and the verbal response simultaneously. In this condition, his pointing ability disappeared,
which suggests that the representative system dominates the implicit action system.

ing. These results suggest that tactile information

510 Vol 6 No3 15 February 1995