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The Neural Basis of Cognition

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Recovery from tactile agnosia: a single case study

Daniela D’Imperio, Renato Avesani, Elena Rossato, Serena Aganetto, Michele

Scandola & Valentina Moro

To cite this article: Daniela D’Imperio, Renato Avesani, Elena Rossato, Serena Aganetto, Michele
Scandola & Valentina Moro (2019): Recovery from tactile agnosia: a single case study, Neurocase,
DOI: 10.1080/13554794.2019.1694951

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Published online: 22 Nov 2019.

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NEUROCASE
https://doi.org/10.1080/13554794.2019.1694951

Recovery from tactile agnosia: a single case study

Daniela D’Imperioa,b, Renato Avesanic, Elena Rossatoc, Serena Aganettoc, Michele Scandolab and Valentina Morob
a
Social Neuroscience Laboratory, Department of Psychology, Sapienza University, Rome, Italy; bNPSY.Lab-Vr, Department of Human Sciences,
University of Verona, Verona, Italy; cDepartment of Rehabilitation, IRCSS Sacro Cuore-Don Calabria, Negrar, Italy

ABSTRACT ARTICLE HISTORY

In a patient suffering from tactile agnosia a comparison was made (using the ABABAB paradigm) between Received 30 August 2018
three blocks of neuropsychological rehabilitation sessions involving off-line anodal transcranial direct Accepted 9 September 2019
current stimulation (anodal-tDCS) and three blocks of rehabilitation sessions without tDCS. During the KEYWORDS
blocks with anodal-tDCS, the stimulation was administered in counterbalanced order to two sites: i) the Tactile agnosia; tDCS;
perilesional parietal area (specific stimulation) and ii) an occipital area far from the lesion (nonspecific parietal lobe; somatosensory
stimulation). deficits; object identification;
Rehabilitation associated with anodal-tDCS (in particular in the perilesional areas) is more efficacious tactile discrimination
than without stimulation.

Introduction
1996), Associative TA is associated with lesions in the infer-
Tactile agnosia (TA) is a modality-specific deficit affecting
ior parietal, supra-marginal gyrus (Platz, 1996; Veronelli,
the tactile recognition of objects, in the presence of ade-
Ginex, Dinacci, Cappa, & Corbo, 2014), the angular gyrus
quate sensory, linguistic and cognitive functions (Bauer,
(Nakamura, Endo, Sumida, & Hasegawa, 1998), the posterior
1993). Patients with TA are unable to identify simple objects
insula and the temporal cortex (Caselli, 1991). A patient
when these are manipulated using the affected hand. In
suffering from TA after a lesion in the corpus callosum
contrast, they can easily recognize the same objects using
(trunk and splenium) has also been reported (Balsamo,
the other hand and when they see them or hear the sound
Trojano, Giamundo, &Grossi, 2008).
they make (e.g., the jingling keys) (Saetti, De Renzi, &
In effect, TA is a rare syndrome, often discussed in
Comper, 1999).
single-case reports (but see Caselli, 1991). To the best of
Following the first anecdotal descriptions of the syn-
our knowledge, there have been no studies to date on the
drome (Lissauer, 1890), TA was subsequently interpreted as
subject which have specifically investigated the possibility
the consequence of sensory disorders (Bay, 1944; Campora,
of rehabilitation by means of specific programs.
1925) but recent studies indicate that itis the result of
Transcranial direct current stimulation (tDCS) offers a
disconnections between the modality-specific encoding for
new method of intervention since it modulates the elec-
tactile sensations and the processes relating to multimodal
trophysiological activity of the brain by means of the
integration (Platz, 1996) or semantic memory systems (Endo,
polarization of neuronal populations (Flöel, 2014). This
Makishita, Yanagisawa, & Sugishita, 1996; Hömke, Amunts,
may potentially be useful in order to facilitate the pro-
Bönig, Fretz,& Binkofski et al., 2009). In some cases (Platz,
cesses of perilesional reorganization, contrast post-lesional
1996; Valenza et al., 2001), the presence of non-efficacious
symptoms due to hyperactivity in some networks or mod-
exploratory motor procedures has suggested that percep-
ulate inter-hemispheric activations (Bolognini et al., 2011;
tual-motor integration may contribute to the syndrome.
Vines, Cerruti, & Schlaug, 2008). Anodal-tDCS increases
Finally, a theory concerning the role of general supra-
cortical excitability with positive effects on learning pro-
modal disorders in spatial perception has also been
cesses (Flöel & Cohen, 2010; Reis et al., 2009) while cath-
advanced (Araneda et al., 2015; Berlucchi, Moro, Guerrini,
odal tDCS has inhibitory effects on neural activity.
& Aglioti, 2004; Caselli, 1991; De Renzi, 1982; Ettlinger,
Here we report the case of a man with unilateral, left-
Warrington, & Zangwill, 1957; Semmes, 1965).
hand TA following a vascular lesion in the right parietal
After elementary sensory perception encoding, the pro-
cortex. Neurological and neuropsychological assessments
cess of object recognition by touch may be compromised at
were associated with an accurate analysis of his lesion.
two steps: i) when sensory elements are integrated
Since our patient was able to perceive simple tactile sti-
(Apperceptive TA) or ii) when the semantic representation
muli, but could not recognize objects as a whole, we
of an object is activated (Associative TA) (Lissauer, 1890).
investigated the effects of anodal-tDCS stimulation on
While Apperceptive TA is reported following damage to the
the perilesional areas. In particular, we addressed i)
inferior parietal and insular cortex (Bay, 1944; Bohlhalter,
whether brain stimulation can enhance the effects of
Fretz, & Weder, 2002; Caselli, 1991; Reed, Caselli, & Farah,

CONTACT Valentina Moro valentina.moro@univr.it

© 2019 Informa UK Limited, trading as Taylor & Francis Group
2 D. D’IMPERIO ET AL.

traditional rehabilitation and ii) whether stimulating two
different sites impacts on the efficacy of the program.
For this reason, we used an ABABAB paradigm, alternating
anodal-tDCS plus behavioral training (A blocks) with a beha-
vioral program (B blocks). In addition, in the A blocks, we
compared the efficacy of tDCS stimulation to two different
cortical areas: i) a specific perilesional area (P4) and ii) a non-
specific area far from the lesion area (Oz-O2). In this way, we
were able to evaluate not only the efficacy of tDCS in beha-
vioral training for TA but also whether its effects are driven by
an increase in neuronal excitability in specific perilesional areas
or by a general cortical activation.
Methods
Case report
US is a right-handed, 56-year-old German man (a fluent speaker
of Italian) with a high standard of education (PhD). After an
ischemic frontoparietal stroke (Figure 1), he complained that he
was no longer able to recognize objects with his left hand,
although he reported that he was able to identify their shape
and size. This deficit could not be attributed to motor deficits (i.
e., there was no hemiparesis or disorders in finger movements)
and it did not affect his right hand.
One month after the lesion onset, an in-depth neuropsycho-
logical assessment confirmed that he did not suffer from
neglect, apraxia, memory or language disorders, although mini-
mal deficits in executive functions were present (Table 1).
Tactile agnosia assessment
In order to isolate TA with respect to sensory deficits, the
Evaluation of Somatic Sensation Test (Smania, Montagnana,
Faccioli, Fiaschi, & Aglioti, 2003) was administered (Table 2).
Although US did not show any left-hand deficits in the detection
of tactile stimuli and somatic sensations (but had some difficul-
ties with tactile extinction and temperature discrimination), he
failed to localize tactile stimuli (with both hands) and to imitate
the position of his right hand with his left hand (Table 2).

Figure 1. US’s lesion.

US’s structural MRI carried out 3 days after stroke was manually mapped on the standard T1-weighted MRI template (ICBM152, Montreal Neurological Institute coordinate system,
approximately matched to the Talairach space) (Talairach & Tournoux, 1988) using MRIcron software (Rorden & Brett, 2000). The template was first oriented on the midsagittal and midcoronal
axis to match the original scan of the patient. Then, an expert clinician (in blind) manually traced the lesion using the MRIcron Software (Moro et al., 2016; Rorden & Brett, 2000). The final image
of the lesion was superimposed onto the Automatic Anatomical Label (AAL) template (Tzourio-Mazoyer, Landeau, Papathanassiou, Crivello, & Etard et al., 2002) to ascertain the number of
voxels involved in the lesion in each area and the center of mass of the lesion. The main areas damaged in the right hemisphere (in red) are the supramarginal gyrus (-x = 53, y = −22, z = 18),
the inferior parietal cortex (x = 37, y = −50, z = 38), the angular gyrus (x = 38, y = −53, z = 22), the rolandic operculum (x = 53, y = −10, z = 11), the postcentral gyrus (x = 63, y = −15, z = 15),
the Heschl gyrus (x = 40, y = −24, y = 12), the superior temporal gyrus (x = 60, y = −12, z = 11) and the insula (x = 41, y = −6, z = 11). The same procedure was used by overlapping the lesion to
the JHU (Johns Hopkins University) DTI-based white matter atlas (Mori et al., 2008) to analyze the white matter tracts. This indicates that the lesion involves the superior longitudinal fasciculus
and the posterior and superior corona radiata. The same test repeated at 10 days from the stroke gave analogous results. The traced lesion (in red) is shown in (a) Axial, (b) Coronal, (c) Sagittal
views and (d) on a 3D brain representation (the right hemisphere is on the right). (e) The tables show the percentage (%) and number (N.) of voxels (Vox) of damaged tissue in each area in the
gray (left table) and white matter (right table). (f) View of the lesion (in red) affecting the white matter. (g) Axial view of the MRI (the right hemisphere is on the right).
 NEUROCASE 3

Table 1. Neuropsychological Assessment. With the aim of determining the type of TA that US was
Cutoff afflicted with (i.e., associative or apperceptive), we capitalized
Score (ES 0–4) on the method of assessment proposed by Veronelli and col-
General cognitive functions
leagues (Veronelli et al., 2014).
MMSE1 30 >24
Attention US was blindfolded during all these tasks, which were first
Trail Making Test2 executed with the left hand and then with the right hand as
Test A (sec.) 50 >93
control (Table 2).
Test B (sec.) 151 >282
Test B-A (sec.) 101 >187
Attentional Matrices3 46.5 30 Tactile recognition
Visual Elevator (TEA4) 8.3 9.2
Stroop Test5 5 different objects were presented at three different time inter-
Word (sec.) 44 <50 vals from the lesion onset in order to verify the stability of the
Color (sec.) 74 <80 symptoms. US was unable to recognize them (15 days: score 1/5;
Color/Word (sec.) 143 <120
PASAT6 25 days: 1/5; 40 days: 2/5; Figure 3(a)), to give any information
ISI 4000 10* ≤6* about their function or to mime their use. Nevertheless, he could
ISI 3000 9* ≤6* describe the shape of the objects in terms of their outline, texture
ISI 1800 24* ≤9*
Spatial neglect and temperature (see supplementary video materials – SM).
BIT7 To verify the patient’s ability to recognize the elementary
Conventional Subtests 141 129 features of the objects, his tactile recognition of geometrical
Behavioral Subtests 80 67
Memory shapes was investigated by means of two tasks. In a same/
Short-term spatial memory3 3.75 3.75 different task (the discrimination of geometrical shapes), US
Long-term spatial memory (Corsi3) 13.9 5.75 was asked to manipulate 12 pairs of three-dimensional geome-
Short-term verbal memory (Word Span3) 2.25 3
Story Recall3 14.4 4.75 trical shapes (i.e., triangles, squares, circles, and rectangles;
Rey 15-words Test8 small = 1.5x1.5 cm; large = 3x3 cm) and to compare their
Immediate Recall 52.2 28.53 sizes and shapes. In a denomination task, the same geometrical
Delayed Recall 13 4.69
Rey Complex Figure Recall9 14.15 6.20 shapes were presented individually and he was asked to name
Imitation hand positions10 20 12 them. US did not any have particular difficulties although his
Apraxia performance with the left hand was not as accurate as with the
Rey Complex Figure Copy11 28.33 28
Clock Drawing Test12 9 7.57 right hand (Table 2).
Ideational Apraxia Test13 14 (4) Finally, the patient performed a Drawing task after haptic
Ideomotor Apraxia Test14 66 53 exploration (Veronelli et al., 2014). In this task, US was asked to
Constructive Apraxia Test3 10.50 (2)
Executive Functions draw an object (with his right hand) after having manipulated it
FAB15 16.8 12.03 (out of sight) with his right or left hand. In cases where there is a
Raven’s progressive Matrices16 36.75 20.72 linguistic deficit, the translation of tactile percepts into a draw-
Tower of London17 23 26.54
WCST18 97.8 90.50 ing should be difficult in both conditions (i.e., right or left hand).
BADS19 In contrast, in the presence of a unilateral agnosic disorder, only
Rule shift cards 0* (4) the object explored by the affected left hand should be inac-
Temporal judgment 3 (3)
Key search 6 (1) curate. US manually explored five different objects (i.e., a birth-
Zoo map 14 (3) day candle, a wooden spoon, a bottle of nail varnish, a pair of
Modified six elements 5 (3) glasses and pincers) and was then asked to draw them imme-
Language
AAT20 diately afterward (using his right hand). After this, in order to
Token test 49 (4) assess his performance, he was also asked to identify the
Repetition 147 (4) objects in his drawings.
Writing 90 (4)
Naming 118 (4) He only found it difficult to recognize his own drawings after
Comprehension 119 (4) manipulating the object with his left hand but did not have any
US’s scores in tests assessing: General cognitive function (1Folstein, Folstein, & problems with his right hand (Left Hand: 2/5; Right hand: 4/5,
McHugh, 1975), Attention (2Giovagnoli et al., 1996; 3Spinnler & Tognoni, 1987; Figure 2).
4
Robertson, Ward, Ridgeway & Nimmo-Smith, 1994; 5Caffarra, Vezzadini, Dieci,
Zonato & Venneri, 2002a; 6Ciaramelli, Serino, Benassi & Bolzani, 2006), Spatial
Neglect (7Wilson, Cockburn, & Halligan, 1987), Memory (8Carlesimo et al., 1996; Praxic ability
Caffarra, Vezzadini, Dieci, Zonato, & Venneri, 2002b. 10Reynolds & Bigler, 1994),
Apraxia (11Reynolds & Bigler, 1994; 12Mondini, Mapelli, Vestri, & Bisiacchi, 2003; A comparison between active and passive manipulation
13
De Renzi, Pieczuro, & Vignolo, 1968; 14De Renzi, Motti, & Nichelli, 1980), allowed us to distinguish between symptoms due to agnosic
Executive functions (15Appollonio, et al., 2005; 16Caffarra, Vezzadini, Zonato, and apraxic deficits. In the active condition, US was asked to
Copelli, & Venneri, 2003; 17Shallice, 1982; 18Laiacona et al., 2000; 19Wilson,
Alderman, Burgess, Emslie, & Evans, 1997) and Language (20Luzzatti et al., identify 12 3D-letters that he was permitted to manipulate
1996) are reported. All scores (second column) are corrected for age and freely. In the passive condition, the same 12 letters were written
education. ES = Equivalent Score. * = tests where the score is based on the by the experimenter on the palm of US’s hands (graphesthetic
number of errors. Pathological ES are 0 (severe) and 1 (moderate). ISI = Inter-
stimuli Interval in msec. Pathological results are in bold; scores at cutoff are in function). In both tasks, US was requested to (i) identify two
italics. letters as being the same or different from each other
4 D. D’IMPERIO ET AL.

Table 2. Clinical assessment of tactile agnosia and correlated functions..

At 1 month At 6 months
Task (number of items) (no. errors) (no. errors)
RH LH LH
Tactile Perception
Lightly touch (12) 100 91.66 (1) 100
Touch with Pressure (12) 100 100 100
Vibration (8) 100 100 100
Temperature (12) 100 75 (3) 100
Tactile extinction (19) 94.7 (1) 84.5 (3) -
Localization of the touch by the other hand (12) 75 (3) 66.66 (4) 75 (3)
Imitation of other hand position (12) 91.66 (1) 50 (6) 75 (3)
Discrimination of movement (12) - 91.66 (1) -
Somatic Sensation Test43
Joint Position Sense (Error 0–51) - 78.43 (11) 84.31(8)
Pressure Sensation (Error 0–16) - 75 (4) 100
Motor Sequences (Error 0–16) - 100 100
Thumb–index grip force control (Error 0–316) - 94.94 (16) 91.14 (28)
Functional tests (Error 0–40) - 100 97.5 (1)
Object recognition (15) 100 26.66 (11) -
Tactile Recognitions17
Geometrical shapes
Discrimination (12) 100 83.33 (2) -
Naming (12) 100 83.33 (2) -
Drawing objects after haptic exploration (5) 80 (1) 40 (3) -
Praxic Abilities17
Letters during active manipulation
Discrimination (12) 91.66 (1) 83.33 (2) 100
Naming (12) 75 (3) 25 (9) 50 (6)
Letters during passive manipulation
Discrimination (12) 91.66 (1) 91.66 (1) 91.66 (1)
Naming (12) 66.66 (4) 41.66 (7) 50 (6)
Supra-modal Spatial Representation17
Tactile Spatial Representation (9) 77.77 (2) 66.66 (3) -
Visual Spatial Imagery
Imagery of letter shape44 (40) 100
The results in the two examinations, before training (at 1 month from lesion onset) and 6 months after lesion follow-up (i.e., 3 months after the end of the training).
Results are reported in percentages of correct responses and number of errors. Sensory perception was assessed by means of clinical tasks and the Evaluation of
Somatic Sensation Test (1Smania et al., 2003). Clinical tests of Tactile Perception, Praxic Abilities and Supra-modal Spatial Representation for the diagnosis of tactile
agnosia were administered following the procedure suggested by 2Veronelli et al. (2014) and 3Sartori and Job (1988). RH = right hand; LF = left hand. * =number of
errors. In parentheses (first column) the number of items per task. For the task involving the imagery of letter shapes, the scores are not hand specific. Pathological
scores are in bold.

(Discrimination task) and (ii) name one of the letters
(Denomination task).
An isolated deficit in identification abilities after active manip-
ulation may be an index of praxic disorders (Valenza et al., 2001),
while in the presence of TA, patients are expected to fail in both
the active and passive conditions (Veronelli et al., 2014). US was
able to recognize whether the pairs of letters were the same or
different both in the active and passive conditions
(Discrimination tasks), and performed with similar results with
both of his hands. The number of errors increased in the
Denomination of letters task in both the active and passive
conditions. Although his performance with the left hand was
worse than that of the right hand, the presence of bilateral errors
may also indicate the presence of spatial deficits (Table 2).
left”). No real difference between the two hands was found
(Table 2), supporting the possibility that some spatial dis-
orders were probably present. In effect, although the task
may be executed by means of semantic, non-spatial strate-
gies (e.g., by counting), US committed errors.
Finally, a test of mental imagery of letters (Sartori & Job,
1988) was administered. In this test, the clinician asks the sub-
ject to describe the lines used to form capital letters in terms of
whether they are curved or straight, vertical or horizontal lines.
US performed without errors.
Considering the results of these tasks as a whole, the pre-
sence of minimal spatial disorders cannot be totally excluded
but this would still not explain the patient’s left-hand agnosic
symptoms.

Supra-modal spatial representation

The presence of spatial neglect had been excluded as a
result of a specific assessment test (Table 1), but we also
assessed Supra-modal spatial representation after tactile
exploration (Veronelli et al., 2014). A 30 × 30 cm base
with 36 nails in it was placed in front of the patient. He
was asked to move one of his hands touching the tops of
the nails according to nine different sets of directions given
by the examiner (e.g., “Please move your hand 3 nails to the
The rehabilitation program
A series of anodal-tDCS stimulation sessions was administered
to US with the aim of investigating its potentially beneficial
effects. In 6 weeks of daily occupational/neuropsychological
rehabilitation sessions (including manual assembly activities,
exercises for attention and executive functions and simple
autonomy tasks involving everyday activities), three 5-day-
blocks of anodal-tDCS stimulation (the A blocks) were

Figure 2. Drawing objects after haptic exploration.
Examples of US’s drawings after tactile exploration of objects. Drawing of a birthday candle after left (a) or right (b) hand exploration. US identified (a) as a little flower and (b) as a birthday
candle. Drawing of glasses after left (c) or right (d) hand exploration.US could not recognize anything in (c), and recognized glasses in (d).
alternated with three 5-day-blocks without tDCS (the B blocks)
but with similar tactile recognition tasks (Figure 3).
In the A blocks, the anodal-tDCS was administered in an off-
line stimulation procedure without any simultaneous behavioral
tasks or stimulation. Specifically, in accordance with safety guide-
lines (Nitsche et al., 2003), off-line anodal-tDCS stimulation was
administered by means of a constant current stimulator
(BrainStim, EMS), using two saline-soaked sponge electrodes (5
× 7 cm; 35 cm2). In each session, the anodal-tDCS lasted 20
minutes (with fade in and fade out of 120 s) at an intensity of
2mA (Hesse et al., 2011; Kim, Lim, Kang, You, & Oh et al., 2010).
The sites of the electrodes were identified following the interna-
tional 10–20 system coordinates (Herwig, Satrapi, & Schönfeldt-
Lecuona, 2003; Jasper, 1958). On each day which included a
stimulation session, the anodal electrode was positioned in two
sites corresponding to the two experimental conditions: the
perilesional parietal area on P4 (the specific stimulation condi-
tion) and the occipital area on Oz-O2 (the nonspecific stimulation
condition). Stimulation in the two conditions was administered
at intervals of at least 2.5 hours and the order of the sites was
counterbalanced across allsessions. The cathodal electrode was
always located in an extra-encephalic position on the contralat-
eral side of the forehead.
NEUROCASE 5
Two different assessments were carried out. The aim of
these was, respectively, to evaluate i) the impact of tDCS sti-
mulation with respect to traditional rehabilitation (i.e., a com-
parison between the A Blocks and the B Blocks, to assess
General Improvement) and ii) any differences in the efficacy
of the stimulation to peri-lesional areas (parietal) with respect
to stimulation to areas far from the lesion (occipital), that is in
order to assess the Specificity of the stimulation site.
In order to test General Improvement, a task involving 12
different objects (i.e., the external assessment list) was used as a
general measure of tactile recognition ability. It was adminis-
tered at baseline, between each individual block (e.g., after A1,
after B1, after A2, etc.) and in two follow-up assessments (at 20
days and 3 months after the end of the training).
To assess the Specificity of the stimulation site, a second test
involving another set with 25 different objects was used across
individual sessions with anodal-tDCS (i.e., only in the A Blocks).
These objects were used to produce various different lists of
objects (5 objects repeated, for a total of 10 objects in each list),
so that each day the difficulty of the objects to be recognized
was balanced and any learning effects due to the repetition
were avoided (see Table 3 for the order in which the lists of
objects were administered).
6 D. D’IMPERIO ET AL.

Figure 3. Experimental Design. (a) Timeline of the entire experiment (6 weeks): 3 weeks of tDCS stimulation associated with traditional occupational/neuropsycho-
logical and motor rehabilitation (A Blocks) were alternated with 3 weeks when the patient participated exclusively in occupational/neuropsychological and motor
rehabilitation, without tDCS stimulation (B Blocks). Before training (baseline), between the A and B blocks and in two follow-ups (20 days and 6 months after the end of
training program), the potential improvement was assessed with a tactile recognition of objects task involving objects which were different from those used during the
training sessions (External Assessment list). Other activities (neuropsychological/occupational activities) were never executed during stimulation but always at different
times in the day. (b) Timeline of an individual tDCS daily session (Block A): the tDCS stimulation was delivered to two different brain areas (i.e., specific – in P4 or
nonspecific – in Oz-O2), in counterbalanced order. Between the two stimulation conditions, there was an interval of at least 2.5 hours. Before and after each brain
stimulation, a tactile object recognition list (different for the two conditions) was used to assess any short-term improvement in performance.

Results follow-ups). This was done by means of the Friedman Test and
repeated Wilcoxon Tests as post hoc analyses.
US’s familiarity with the objects was confirmed by his perfor-
mance with his right hand (accuracy = 93%).
Due to the fact that the number of objects was small and the Table 3. The lists of objects used to assess the effects of anodal-tDCS (A blocks)
data were ordinal in nature, non-parametric analyses were and the order of administration is schematized.
computed and the effect size r was adopted (r ≤ 0.05 = no Specific Parietal Nonspecific Occipital
A Blocks stimulation stimulation
effect, 0.1 ≤ r ≤ 0.23 = small effect, 0.24 ≤ r ≤ 0.36 = intermedi- (5 days per week of tDCS) condition condition
ate effect, r > 0.37 = large effect) (Cohen, 1988). All scores were A1 (10 objects) List List
blindly assigned after the end of the task by two examiners Day 1 A F
based on a recording of the patient’s responses. Day 2 B G
Day 3 C H
Day 4 D I
Day 5 E L
General improvement A2 (10 objects)
Day 1 F A
In order to verify the results of the program as a whole, the Day 2 G B
Day 3 H C
functional strategies used by the patient in order to recognize Day 4 I D
the object were considered in order to record his performance. Day 5 L E
In fact, although in some cases an improvement was seen in A3 (12 objects)
Day 1 M N
correspondence with the correct recognition of an object, at Day 2 O P
other times he deduced the nature of the object by means of Day 3 N M
resorting to other information resulting from his tactile explora- Day 4 P O
Day 5 Q R
tion. A comparison was made between the raw scores for each
Each list was composed of 5 objects repeated once (10 objects in total), except for
object (0 = failure to recognize; 0.5 = recognition of the correct block A3 which involved 6 objects repeated once (12 objects in total) in order to
semantic category – e.g., the typical use or the place where the increase the number of trials according to US’s improvement. The same list was
object is usually found; 1 = correct recognition) with reference administered before and after a single session of anodal-tDCS, but the lists were
different within each day for the two conditions of tDCS (in different stimulation
to the external assessment list of objects in the various different sites) and were randomized across all weeks. Capital letters indicate which lists
phases of the programme (Baseline, A1, B1, A2, B2, A3, B3, two were used.

The results of the comparison were significant (χ2(8) = 21.37,
p < 0.01, effect size r: 0.77). At the post-doc analyses, significant
differences in the baseline with respect to A3 (Z = −2.07, p =
0.02, r = 0.59) and B3 (Z = −1.89, p = 0.04, r = 0.54) were found.
The improvement in performance lasted until the first (Z =
−2.18, p = 0.02, r = 0.63) and second follow-ups (Z = −1.95, p
= 0.04, r = 0.56) (Figure 3(b)). In addition, significant differences
emerged in the comparisons between the first follow-up versus
A1 (Z = −2.20, p = 0.03, r = 0.63) and B1 (Z = −2.02, p = 0.053, r =
0.58) (Figure 4).
Effects of stimulation
In order to assess the patient’s performance with reference
to the presence as compared to the absence of tDCS, the
effects of rehabilitation in the individual A blocks (with
tDCS) were compared to those relating to the B blocks
(without tDCS) by means of a Wilcoxon test. For each
block, the analysis was computed on the differences
between the scores for the external assessment list of
objects in the post-block and those for the respective pre-
vious assessment (i.e., the differences between post-A1v.
Baseline, post-B1 v. post-A1, post-A2 v. post-B1, etc.). For
each object, a performance index was calculated: +1 or +0.5
= the patient identified correctly or partially correctly an
object which had not been identified in the previous
block; 0 = performance did not change; −1 or −0.5 = he
failed to recognize an object which had been previously
correctly or partially correctly identified.
The Wilcoxon test showed that the patient’s performance
was better in the blocks after tDCS (i.e., the A blocks) than
those without tDCS (i.e., the B blocks) (Z = −1.87, p = 0.054,
r = 0.31).
Specificity of the stimulation site
In order to investigate any potentially different effects relating
to the site being stimulated, a further analysis was computed
on the A blocks. By means of a repeated Wilcoxon test, a
Figure 4. Measures of Stability of symptoms and General Improvement. (a) US’s performance in object recognition tasks in three sessions before the experimental
procedure as a measure of stability of symptoms (see “Tactile recognition“ section), (b) General improvement: analysis of performance after each training block (with
A1, A2, A3 and without tDCS B1, B2, B3) and in the two follow-ups. *:<0.05.
NEUROCASE 7
comparison was made between the number of objects recog-
nized after specific and nonspecific stimulation (Parietal vs.
Occipital sites). For each session, the scores related to the
differences between the recognition of objects before and
after tDCS stimulation (with the values for the performance
index as described in the Effects of stimulation section).
The results indicated that tDCS applied to the specific, peri-
lesional Parietal area was globally more efficacious than non-
specific stimulation applied to the Occipital cortex (Z = −2.00, p
= 0.046, r = 0.38).
For each stimulation site (i.e., specific and nonspecific), the
three blocks were further compared by means of a Friedman
Test (Time: first, second, third). Although the results were not
significant, in the specific Parietal Stimulation Site Condition
the improvement was different between the three blocks
(Friedman χ2(2) = 5.80, p = 0.05, r = 0.13) (Figure 5).
Discussion
In this single case study, an in-depth neuropsychological
assessment of a patient affected by TA was carried out. In
addition, the effects of tDCS on the symptoms were investi-
gated. The results indicate that tDCS enhanced US’s perfor-
mance in tasks involving the tactile recognition of objects and
that perilesional Parietal stimulation is more efficacious than
stimulation to a nonspecific Occipital area.
Phenomenology and neural correlates of TA
The patient US presented with left hand unilateral TA (Lissauer,
1890).A neuropsychological assessment allowed us to exclude
the possibility that US’s symptoms directly depended on tactile,
motor, language or spatial representation disorders, although
minimal spatial disorders were probably present.US was not
impaired in the recognition of the size and shape of objects
(morphoagnosia) or in the discrimination of specific features
relating to objects, such as the weight, texture or temperature
(hyloagnosia) (Delay, 1935), thus excluding a main role of his
sensory-motor and praxis minimal disorders. He was also able
8 D. D’IMPERIO ET AL.
Figure 5. Measure of Specificity of the stimulation site. Differences between post and pre stimulation are reported with the comparison between the scores relating to
Parietal (specific) and Occipital (nonspecific) stimulation in the three blocks involving stimulation to each site. Significant direct contrasts are reported. * = 0.038, effect
size: r = 0.16.
to describe objects in detail after manipulation with his left
hand. Nevertheless, US showed relevant deficits when integrat-
ing tactile elements in order to achieve object recognition and
could not denominate or describe objects or mime their
function.
An analysis of the patient’s lesion supported the diagnosis as
TA symptoms are usually due to a disconnection between the
primary somatosensory cortex and the networks involved in
the higher order cognitive processes associated with object
identification (Platz, 1996), or between these latter and the
semantic memory system (Endo et al., 1996).
In line with previously reported cases of Associative TA
(Caselli, 1991; Nakamura, Endo, Sumida, & Hasegawa, 1998;
Platz, 1996; Veronelli et al., 2014), US’s brain damage mainly
involved the right hemisphere in the supramarginal gyrus, the
inferior parietal cortex, the angular cortex, the insula and the
temporal cortex.
However, similarly as with other previously reported cases of
Apperceptive TA, US’s brain damage also involved the inferior
parietal cortex and insula (Bay, 1944; Bohlhalter et al., 2002;
Caselli, 1991; Reed et al., 1996). These results are consistent with
the neuropsychological data indicating a mixed form of TA.
Furthermore, the patient’s lesions involved the subcortical
white matter, in particular the posterior and superior corona
radiate and the superior longitudinal fasciculus. This connects
the posterior and anterior networks pertaining to attentional
processes (Bartolomeo, de Schotten, & Doricchi, 2007; de
Schotten et al., 2011) and damage to this area might explain
the dysfunctional signs relating to executive functions. These
subcortical lesions may also have damaged the connections
between the parietal (SII, inferior parietal and posterior asso-
ciative areas) and frontal (prefrontal, SMA, premotor, FEF) cor-
tices, which are active in normal people during tactile
recognition tasks (Crutch, Warren, Harding, & Warrington,
2005; Platz, 1996; Reed, Shoham, & Halgren, 2004; Valenza et
al., 2001).
There is thus a distributed neural network underlying the
complex system relating to tactile recognition. In two
previously described patients, the connections between the
posterior parietal lobe and the post-central gyrus turned out
to be relevant to the processing of tactile elements from a
parallel perception of individual elements to their serial asso-
ciation and the identification of the object in question, respec-
tively (Bohlhalter et al., 2002).
Finally, a ventral pathway (connecting SI, SII, insula and
medio-temporal areas) is involved in the nonspecific modality
of object recognition, as shown in memory tasks involving the
recognition of the shape of objects (Bonda, Petrides, & Evans,
1996), object discrimination (Saetti et al., 1999) and the integra-
tion of different modalities in object recognition (Bay, 1944).
The effects of tDCS
The application of tDCS in rehabilitation programs is relatively
recent and to date only a few studies have investigated the
efficacy of this stimulation when associated with a specific
rehabilitation program for brain-damaged patients (e.g.,
Boggio et al., 2007; Bolognini et al., 2014, 2011; Làdavas,
Giulietti, Avenanti, Bertini, & Lorenzini et al., 2015; Rocha et
al., 2015). In line with these previous studies, we chose to
administer repeated tDCS sessions in order to monitor the
additive effects of stimulation (Bolognini et al., 2011; Rocha et
al., 2015) in a rehabilitation program. In addition, we assessed
the impact on US’s performance by comparing his results after
the application of tDCS to two different stimulation sites.
The results of the present study show that in the case of this
patient, tDCS enhances the effects of rehabilitation, with pro-
longed long-term effects. These were also confirmed by the
patient himself who reported an improvement in daily life
activities, in particular during bimanual actions and in tactile
investigations of objects. The possibility of a spontaneous
recovery is excluded as US’s deficits were stable at the three
measurements of baseline. It is to be further noted that he
carried out identical rehabilitation activities in the A and B
blocks (i.e., with occupational/neuropsychological rehabilita-
tion) and that the tDCS stimulation (only in the A blocks) was

administered off-line without any simultaneous tasks. It may
thus be inferred that any improvement in the A blocks with
tDCS was not influenced by other exercises.
We consider that the tDCS program was relatively long. This
may have facilitated some processes of long-term potentiation
(LTP) (Brunoni, Nitsche, Bolognini, Bikson, & Wagner et al., 2012;
Liebetanz, Nitsche, Tergau, & Paulus, 2002; Nitsche, Cohen,
Wassermann, Priori, & Lang et al., 2008; Stagg & Nitsche, 2011)
with a plastic perilesional reorganization of neural networks.
Post stimulation effects have been reported elsewhere
(Nitsche & Paulus, 2000), but we exclude any potential effects
of adaptation to stimulation since the improvement gained by
the subject in our study was maintained, even though our
paradigm included long intervals without tDCS (1-week blocks
– B1, B2 and B3) (Nitsche& Paulus, 2000; Siebner, Lang, Rizzo,
Nitsche, & Paulus et al., 2004).
Another interesting result arose from the comparison that
was made between the two stimulation sites indicating that
tDCS is more efficacious when applied to the perilesional
Parietal area than the Occipital area. This is in line with other
recent studies that discuss the importance of focused stimula-
tion (Woods et al., 2015) and the utility of intervening on the
reorganization of perilesional networks rather than on far from
lesion circuits.
The absence of a proper “sham” condition (i.e., fake tDCS
stimulation) was due to two factors: i) US’s high sensitivity to
any changes in tDCS intensity and ii) the desire to focus on the
neural network of activation with a view to comparing two
areas of interest in without other individual variables (for a
discussion, see Fertonani &Miniussi, 2017). This is in line with
the recent debate on the advisability of comparing various
different target areas of stimulation, which may reveal the
importance of a specific localized stimulation versus a control
area (Ellison, Lane, & Schenk, 2007).
In particular, P4 (PPC) is a stimulation site which has been
previously used, in particular in the rehabilitation of neglect
(Làdavas et al., 2015) and apraxia (Bolognini et al., 2014). PPC
corresponds to the area between the superior and inferior
parietal cortices in the parietal-frontal network which is often
disconnected in TA (Caselli, 1991, 1993; Reed & Caselli, 1994;
Reed et al., 1996). Indeed, patients with apperceptive TA pre-
sent mainly post-central gyrus and SII lesions, but also more
posterior parietal damage in relation to more severe deficits
(Bohlhalter et al., 2002). Furthermore, right posterior parietal
regions are reportedly involved in the development of spatial
abilities, and are susceptible to specific neurodegeneration
(focal progressive disease, see Miller et al., 2018). For this rea-
son, we suggest that stimulation to PPC might have modulated
the increased activity and plastic processes of reorganization in
the spared areas around the lesion, but we cannot exclude the
possibility that the amelioration in tactile agnosia is at least in
part mediated by an improvement in the networks involved in
spatial functions as well.
Nevertheless, it has been suggested that PPC also has a role
in the recognition of an object in other (non-tactile) sensory
modalities since it is involved in the integration of the various
different features of the object (Ellison et al., 2007). In tactile
discrimination, similar results for tDCS stimulation are reported
for vibration and painful stimulation (Antal et al., 2008;
NEUROCASE 9
Dieckhöfer et al., 2006; Fujimoto, Yamaguchi, Otaka, Kondo, &
Tanaka, 2014; Matsunaga, Nitsche, Tsuji, & Rothwell, 2004;
Ragert, Vandermeeren, Camus, & Cohen, 2008; Rogalewski,
Breitenstein, Nitsche, Paulus, & Knecht, 2005; Terney et al.,
2008). Finally, a study on chronic stroke patients with sensory
deficits showed that they made improvements in tactile spatial
discrimination after dual-hemisphere tDCS stimulation over S1
and S2 (Fujimoto et al., 2016).
In conclusion, the main aim of our study was to expand on
the results from previous studies on the discrimination of simple
tactile stimuli and, to the best of our knowledge, this is the first
attempt to apply a specific tDCS program in TA and the first to
provide evidence that it may be possible to ameliorate the
symptoms with a combination of specific tDCS stimulation and
behavioral rehabilitation. Further investigations into tDCS as a
means of aiding recovery from TA are needed in order to clarify
the role of the other areas in the complex cortical and subcor-
tical frontoparietal network which are involved in tactile
recognition.
The study has some limitations. The first is that it involves
only one individual patient due to the rarity of the syndrome,
meaning that only a within-subject comparison was possible.
Nevertheless, US’s TA was stable at the beginning of the inter-
vention, thus excluding the hypothesis of a spontaneous recov-
ery. Moreover, it appears that the association of tDCS with the
contemporary execution of specific tasks can potentially
increase the efficacy of treatment, driving the neuromodulation
induced by stimulation toward the network actually involved in
the tactile task. Further studies are needed to better under-
stand the potential of tDCS in clinical practice.
Acknowledgments
We wish to thank US and his relatives for their kindness and their willing
participation in our study.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the University of Verona [Bando di Ateneo per
la Ricerca di Base 2015];Ministero dell’Istruzione, dell’Università e della
Ricerca [Progetti Di Ricerca Di Rilevante Interesse Naziona];CEMS, Verona
[Verona Memory Center].
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