1662
ORIGINAL ARTICLE
Assessing Subclinical Tactual Deficits in the Hand Function of
Diabetic Blind Persons at Risk for Peripheral Neuropathy
David Travieso, PhD, Susan J. Lederman, PhD
ABSTRACT. Travieso D, Lederman SJ. Assessing subclinical tactual deficits in the hand function of diabetic blind
persons at risk for peripheral neuropathy. Arch Phys Med
Rehabil 2007;88:1662-72.
Objective: To assess subclinical impairments in tactual hand
function produced by diabetes mellitus in late-blind adults with
diabetic retinopathy.
Design: The survey compares diabetic blind with nondiabetic blind and blindfolded sighted controls in terms of their
performance on a battery of tests that assess tactual hand
function.
Setting: Subjects were evaluated at their rehabilitation program center in Madrid.
Participants: Nine (referred) diabetic blind subjects affected by diabetic retinopathy versus 10 (referred) nondiabetic
blind subjects versus 10 blindfolded sighted volunteers, all
right-handed and matched for age. Subjects were referred by
the training professionals of the rehabilitation program center
and asked to volunteer.
Interventions: Not applicable.
Main Outcome Measures: Cutaneous force and spatial
resolution thresholds, haptic psychophysical functions for perceived roughness, weight, and size, and both accuracy and
response times for haptic classification of 3-dimensional common objects. Measures of joint mobility, muscular strength,
and motor dexterity were also included.
Results: The diabetic blind performed significantly poorer
than the controls in terms of force sensitivity (distal and proximal finger pads, and palm), spatial resolution (distal finger pad
only), motor dexterity, perceived roughness, and finally, haptic
object classification response times for texture-diagnostic
objects.
Conclusions: Subclinical disturbances in the tactual hand
function of the diabetic blind subjects were only documented in
perceptual and motor tasks for which cutaneous, as opposed to
kinesthetic, information was particularly relevant.
Key Words: Blindness; Diabetic neuropathies; Disability
evaluation; Hand; Rehabilitation; Touch.
© 2007 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and
Rehabilitation
From the Facultad de Psicología, Universidad Autónoma de Madrid, Spain (Travieso); and Department of Psychology, Queen’s University, Canada (Lederman).
Supported by the Spanish Ministerio de Educación y Ciencia (grant nos. BFF20030129, HUM2006-11603-C02-02) and the Canadian Institutes for Health Research.
No commercial party having a direct financial interest in the results of the research
supporting this article has or will confer a benefit upon the authors or upon any
organization with which the authors are associated.
Reprint requests to Susan J. Lederman, PhD, Dept of Psychology, Queen’s University, Kingston, ON K7L 3N6, Canada, e-mail: [email protected].
0003-9993/07/8812-11616$32.00/0
doi:10.1016/j.apmr.2007.09.007
Arch Phys Med Rehabil Vol 88, December 2007
T IS WELL KNOWN THAT the retinopathy caused by
Iness.diabetes
mellitus is one of the main causes of adult blindProfessionals who deal with blind diabetic adults usu1,2
ally report tactual disturbances that clearly impede the process
of rehabilitation and training of tactual function.3 The diabetes
literature shows that in its latest stages, diabetes produces
disturbances in peripheral nerves that can terminate in peripheral neuropathy, most commonly resulting in sensory deficits in
limb extremities that advance in a distal-to-proximal direction.3-6 In contrast to the more extensive literature on sensorimotor function of the lower extremities,7,8 the functional impact of peripheral neuropathy on the sense of touch in the upper
extremities (also including hand dexterity and Braille reading9-11) has been studied very little. Moreover, the number and
types of tests have been relatively restricted, given what is now
known about tactual hand function.12 The tests have typically
included determining thresholds for vibration and/or thermal
sensitivity, and sometimes, for force (usually misnamed as
“pressure”) sensitivity and spatial resolution. It is intriguing,
however, that several studies have reported sensory deficits that
precede the clinical onset of peripheral neuropathy,4,13 including higher cutaneous thresholds in the fingertips and disturbances in peripheral nerve conduction.4,5,14 The purpose of this
research, therefore, was to expand the assessment tests of
subclinical impairments in tactual hand function produced by
diabetes mellitus in late-blind adults with diabetic retinopathy.
For this subpopulation of diabetics, the negative consequences
of impaired tactual hand function pose critical problems for
rehabilitation and re-education with respect to many daily
manual activities, including Braille reading. Such emphasis on
the upper extremities in blind diabetics contrasts with sighted
diabetics for whom the diabetic foot constitutes a more serious
problem.
To expand on our statement above, the sense of touch is
considerably more complex than the diabetes literature has
addressed to date. First, although recognized as a critical component of normal tactile hand function,12 spatial resolution has
scarcely been addressed. In addition, there is considerably
more to touch than the internal punctuate sensations that are
based on inputs from the cutaneous (tactile) system. Our sense
of touch is also used to experience the complex world of
external objects.12,15,16 For such purposes, the field of experimental psychology emphasizes the critical contributions of
haptics, an additional subsystem that uses combined sensory
inputs from both cutaneous and kinesthetic systems. To further
clarify, from a functional point of view, the cutaneous system
provides information about stimulation of the external surface
of the body via mechano- and thermoreceptors embedded in the
skin. The kinesthetic system provides information about the
position and movement of the limbs via activity in mechanoreceptors in muscles, tendons, and joints (and in hand skin).
The integration of the inputs from these 2 subsystems is
achieved via the haptic system, which combines both cutaneous and kinesthetic sensory cues, typically by means of voluntary manual exploration, to produce complex perceptions of
external objects and their properties.17
TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
In the current study, we therefore assessed the tactual hand
function of diabetic blind adults at risk for peripheral neuropathy using a more comprehensive battery of tests than has past
research. Rather than focusing narrowly on cutaneous sensitivity to vibration and/or temperature, we addressed other potentially important aspects of tactile sensing in the hand, namely,
force sensitivity and spatial resolution, and for the first time,
haptic perceptual functions.
More specifically, we evaluated tactile sensing by evaluating
force thresholds (ie, inverse of force sensitivity), and spatial
acuity thresholds (ie, the inverse of spatial resolution) for
2-point touch (both static and moving), and point localization
tasks. We also assessed the more complex haptic perceptions of
object properties, including texture, weight, and volume. Finally, we assessed the constrained haptic classification of common objects. To assist in interpreting haptic performance, we
evaluated musculoskeletal function using tests of joint mobility
and muscular strength, and manual dexterity using tests of fine
and coarse motor control. For each test, we compared the
performance of diabetic blind subjects with that of both nondiabetic blind and blindfolded sighted controls. Inclusion of the
nondiabetic blind group allowed us to assess the additional
tactual impairments in sensation and perception that were the
consequence of subclinical peripheral neuropathy in those who
were already blind. The sighted control group provided a
baseline for those without either diabetes or blindness.
Based on the previous literature reporting distal-to-proximal
impairments in cutaneous function in diabetics with preclinical
or actual peripheral neuropathy, we predicted that tactile sensing (ie, cutaneous thresholds) would be more impaired (ie,
higher) than either control group. Moreover, because the sense
of touch includes haptic sensing as well, to the extent that
kinesthetic function was relatively intact in the diabetic blind
group, we predicted that their performance on haptic perception tasks involving perceived magnitude of weight and volume
would be similar to the control groups, because neither type of
percept depends primarily on intact cutaneous information. In
contrast, we predicted that performance of tactual functions
that relied extensively on cutaneous information (ie, perceived
magnitude of texture, identification of common objects for
which texture is most diagnostic) would be impaired relative to
the control groups.
METHODS
The ethics procedures prescribed by both CERBVO (Special
Center for General and Visual Rehabilitation of the Spanish
National Organization for the Blind) and the Universidad Autónoma de Madrid were followed.
Participants
Three groups of subjects participated. The experimental
group consisted of 9 diabetic late-blind subjects. The blindness
etiology for all subjects in this group was diagnosed by a
professional as diabetic retinopathy. They had been diabetic for
an average of 22.5 years and totally blind for an average of 8
years. None of this group was diagnosed with peripheral neuropathy, reported pain, or gave any evidence of cognitive disorders as
measured by a brief, portable mental status questionnaire.18 The
first control group included 10 nondiabetic late-blind subjects. All
blind subjects were registered in CERBVO in Madrid, Spain,
where they followed rehabilitation and training programs and
were asked to voluntarily participate in the study. The second
control group included 10 blindfolded, sighted subjects, who were
recruited in the Fuencarral neighborhood in which the Autonomous University is situated. They were recruited through private
1663
and public advertising. All 29 subjects were right-handed, as
determined by the Edinburgh Inventory,19 and were matched for
age. Poor musculoskeletal function was considered an exclusionary criterion; however, only 1 person was rejected due to arthrosis,
which prevented her from producing full hand flexion and extension. A complete description of the 3 groups is presented in
appendix 1.
Materials
In the next section, we discuss the battery of tests that were
used together with reasons for their inclusion.
Musculoskeletal hand function: joint mobility and muscular strength. The joint tests consisted of hand flexions (both
hands) and included those regularly used in clinical observation
(ie, hand flexion and extension, digital flexion, lateral flexion of
thumb to lateral base of the index finger, thumb-index opposition, thumb-little finger opposition, and thumb to little finger
base flexion). The tests determined the participant’s greatest
joint movement relative to norms for maximum passive and
active joint function, which were measured in terms of either
linear or angular extent.20 In our case, the linear extent of the
gap between fingers for the different flexions was measured
using a ruler, whereas the angle for full extension was measured with a goniometer. For purposes of the current experiment, we included only participants who showed normal function, that is, full flexion and extension. This was done to ensure
that performance on any haptic task was not impaired because
of reduced musculoskeletal hand function. The muscular
strength tasks measured maximum effort21 for 5 different handgrips: fist, lateral, thumb-index, thumb-index/middle, and
thumb-little. Subjects were required to press 5 hand tendersa
with different resistances. Muscular effort was measured in
kilograms.
Cutaneous force sensitivity and cutaneous spatial resolution. We used 4 psychophysical tests of cutaneous hand function: force sensitivity, and 3 tests of spatial resolution, including static 2PT threshold (static 2PT), moving 2-point touch
threshold (moving 2PT), and point localization. Although
moving 2PT and point localization thresholds are not regularly
measured in the diagnosis of diabetic neuropathy, they were
included in the current study because they provide a more
comprehensive evaluation of perceptual hand function. The
force threshold was determined using Semmes-Weinstein
monofilaments. The spatial resolution tests were performed
using an aesthesiometer for static 2PT, moving 2PT, and point
localization. As mentioned earlier, more is known about vibrotactile and thermal sensitivity, which have traditionally been
evaluated as diagnostic tests of diabetic peripheral neuropathy.1
Accordingly, they were not included in the current study,
which selected other tests not commonly used in this field.
Another reason they were excluded is that such tests have not
been used as a predictor of functional capabilities (eg, manual
dexterity, haptic object recognition12).
Motor dexterity. Although we documented no significant
differences in either joint mobility or muscular strength among
our 3 groups, several studies with diabetic10 and nondiabetic
populations22-24 have found that impairments in tactile sensory
and haptic perceptual performance do affect manual dexterity.
Accordingly, our subjects also performed 2 tests of motor
dexterity. It is important to note that none of the tests used here
has been previously standardized for use with blind populations; therefore, we compared results among groups without
referring to standardized test norms.
The Moberg Pick-up Test25 evaluates fine motor dexterity
for hand rehabilitation of patients who have undergone hand
surgery. It consists of a square plastic box, with dimensions
Arch Phys Med Rehabil Vol 88, December 2007
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TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
5⫻5⫻1cm. The object set includes 12 small common objects
that fit within the box, including screw, nail, paper clip, safety
pin, coin (diameter, 1.0cm), small button (diameter, 0.7cm),
nut (shaft diameter, 0.8cm), padlock key, washer, spike, large
button (diameter, 2.0cm), and coin with a central circular hole
(diameter, 2.0cm; hole diameter, 0.5cm).
The Minnesota Rate of Manipulation Test (MRMT) is a
standardized test for evaluating relatively coarse hand dexterity, as, for example, when assessing personnel performance on
assembly lines. The MRMT uses a board (90⫻30cm) with
circular holes for introducing 60 cylindrical pieces (each 4cm
in diameter and 2cm high).
Haptic scaling of the physical magnitude of object dimensions. Participants performed 4 separate scaling tasks that
required them to haptically estimate magnitude along 4 different perceptual dimensions: surface texture (roughness), weight,
volume (cubes), and volume (spheres). The experimental levels
for each dimension were preselected on the basis of a preliminary 2-alternative forced-choice signal detection theory experiment performed with 10 blindfolded, sighted subjects. These
data permitted us to select stimulus values with high detectability between adjacent stimulus pairs (ie, d=⬎1.5) that when
used in a category-scaling task produced psychophysical functions that may be described with linear functions fitted to the
data. In addition, the discriminability levels were similar across
the different magnitudes considered (d= range, 1.5⫺2.5). Ten
values were selected for each object dimension, which included
texture, weight, and 3-dimensional volume (cubes, spheres).
The textured surfaces consisted of 10 plates of raised 2-dimensional spatially jittered dots, with the mean inter-dot distance
within each plate increasing across plates from 0.50 to 2.75mm
in increments of 0.25mm. The weight stimuli consisted of 10
cylinders increasing from 50 to 275g in increments of 2g. The
3-dimensional volume stimuli consisted of 10 cubes varying
from 48 to 120cm3 in increments of 8cm3, and 10 spheres with
variations in diameter from 13 to 60mm.
Three-dimensional common-object identification task. The
final task used in the current study was still more complex,
involving the haptic identification of multi-attribute common
objects. A set of 30 objects was selected on the basis of a study
by Lederman and Klatzky,26 in which subjects were required to
identify objects, each selected on the basis of a highly diagnostic property (eg, texture is diagnostic of sandpaper). We
were interested in whether impairments in simple manual sensory and/or motor functions would affect haptic identification
of common objects in terms of response accuracy and/or response time. The current set was grouped into 6 subsets of 5
objects, each subset defined by a different highly diagnostic
property at either the basic (eg, spoon) or subordinate (eg, soup
spoon) level of classification.27 The 6 diagnostic properties
included size, form, texture, temperature, weight, and hardness.
The stimulus objects and associated diagnostic property are
listed in appendix 2.
Experimental Procedures and Designs
Subjects performed the battery of tests in 3 sessions. In
session 1, subjects were sequentially evaluated for joint mobility, muscular strength, force sensitivity and spatial resolution. In session 2, they haptically estimated the magnitude of
texture, weight, and volume (cubes, spheres). In session 3,
subjects performed the 2 motor dexterity tests and the 3-dimensional object-classification task.
Musculoskeletal hand function: joint mobility and muscular strength. Before the formal experiment began, subjects
performed standard tests of musculoskeletal hand function.
First, they were asked to perform a set of manual joint mobility
Arch Phys Med Rehabil Vol 88, December 2007
actions, specifically hand flexions and extension. Normal function was required in order to participate in the study. Muscular
strength tests were performed to confirm that subjects’ performance on motor dexterity and perceptual tests requiring intact
motor function were not affected by muscular impairment.
More specifically, subjects performed a set of hand grips with
tenders. The results were compared among groups to ensure
that there were no significant differences in muscular strength
among them.
Cutaneous force sensitivity and cutaneous spatial resolution. In keeping with Weinstein,28 we assessed thresholds
using a modified method of limits with 3 ascending and 3
descending series presented in alternation. For force thresholds,
the diameter of the monofilaments was increased (decreased)
until the subject first detected (failed to detect) the stimulus.
The mean of these 6 momentary thresholds was used as the
force threshold for the given site. For static and moving 2PT
thresholds, for presentation of a double stimulus, the 2 tips of
an aesthesiometer (like a machinist’s calipers) were applied to
the skin as simultaneously as possible along the longitudinal
axis of the finger and hand. For catch trials, a single point
stimulus was used with the same total area as those of the 2 tips
of the aesthesiometer. For the static 2PT threshold, the points
remained in place on the skin; for the moving 2PT threshold,29
the 2 prongs were moved along the skin. For each 2-point
separation value, the subject was required to identify 2 double
and 2 single points presented in random order. The separation
between the 2 points was increased or decreased in 0.2-mm
intervals until the subject made a mistake (ie, perceived 2
points in a catch trial or 1 point when 2 points were applied).
The mean of the 6 momentary thresholds was used as the
threshold for that condition. The point localization thresholds
were determined by applying a single point along each of 3
arms (both distal and proximal directions) of a Y-shaped grid
drawn on the skin. The arms were separated by 120°. Gradations of 0.2mm were used. The center of the grid was touched
firmly and described as the “reference point.” Following stimulation of the center point, the comparison points of the arm
being tested were touched. The subject was asked to say
whether it was the reference point or not. Series of proximal
and distal directions with respect to the center point were
alternated on each of the 3 arms. The point that was called the
reference point that was furthest from the center was determined for each of the 3 arms. The mean of these 3 values was
used to calculate the error of localization.
Each subject performed the 4 tests of cutaneous sensitivity
and spatial resolution in random order. Force thresholds were
measured in grams; the 3 tests of spatial resolution were
measured in millimeters. Separate thresholds were obtained in
the center of the distal finger pad (fingertip) of the thumb, index
and little fingers, the proximal finger pad of the index and little
fingers, and the center of the palm. While the hand rested on an
armchair, the stimuli were applied with sufficient force to just
produce skin deformation.
Manual dexterity. The Moberg Pick-up Test was performed separately with each hand. The subject picked up the 12
small objects, one at a time, and placed them into a small box.
As each object was lifted up, the subject was required to name
it. They performed the entire task with each hand in 2 separate
blocks, with the order in which the hands were used randomly
selected for each subject. The order in which the objects were
presented within each hand block was also randomized. The
objects were laid out on a towel in a 10cm round space and the
experimenter placed the subject’s hand over the set of objects.
Subjects used their free hand to hold the box in place. Both the
TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
left and right hands were tested. The dependent variable was
response time in seconds.
Each subject also performed 3 subscales of the MRMT. Two
of these required using the left or right hand to transfer the
cylindrical objects arranged on the board, from 1 hole to the
adjacent empty one, as quickly as possible. The top left hole
was removed to start, and the task finished when the bottom left
hole was emptied and the block inserted in the adjacent hole.
The third subset required subjects to remove the blocks from
the holes in the test board with 1 hand, turn them over with the
other hand, and replace them in the same holes, proceeding
from 1 block to the next as quickly as possible. Response time
was measured with a stopwatch in seconds from initial contact
with the first cylinder until the final one was inserted into the
hole. Each subject performed 1 practice trial and 3 experimental trials during which response time was measured. The order
in which the 3 subscales were performed was randomized for
each subject.
Haptic scaling of the physical magnitude of object dimensions. We asked subjects to evaluate the perceived magnitude
of texture (described as “spatial density,” ie, the number of dots
in each plate), density (described as “weight”) and volume
(described as “size”) using the category-rating procedure described by Ward et al.30 Subjects were told that there were 10
objects on each dimension. The objects with the lowest and
highest levels on each dimension were presented to the subjects, and described with values of 1 and 10, respectively. Then
1 training trial and 5 experimental trials were performed. On
each trial, a stimulus was placed on the subject’s hands, and the
subject was allowed to freely explore each object with no time
limit. Subjects then rated each of the 10 stimuli on a scale of 1
to 10 to indicate the perceived position of each stimulus within
the series for each dimension. The 10 stimuli for each dimension were presented in random order within each block. There
were 5 repetitions per block for each dimension. The order in
which the 4 dimensions were presented was randomized for
each subject.
Haptic identification of 3-dimensional common objects. Subjects were seated in front of a desk covered with a towel in
order to eliminate any acoustic clue to object identity. Subjects
were asked to answer a question about the object after it was
placed in their hands. They were free to explore the objects as
they wished, but had to answer the following question as
quickly and as accurately as possible: “Is this X also a Y,”
where “X” was named at the superordinate (eg, abrasive surface) or basic (eg, sandpaper) level, and “Y” was correspondingly named at the basic or subordinate (eg, rough sandpaper)
level. A binary response (yes, no) was required. There were a
proportional number of positive and negative questions for
each diagnostic property at each classification level. The 30
objects were presented in random order. Response time was
measured manually in seconds.
RESULTS
Musculoskeletal Hand Function: Joint Mobility and
Muscular Strength
All tests were performed accurately with the exception of 1
subject who was rejected because of arthrosis, which prevented
her from executing full flexion and extension of the hand. All
other joint mobility tests were performed normally; that is,
each subject in each group performed both full flexions and full
extensions. A 3-factor mixed analysis of variance (ANOVA),
with perceptual status (3 levels), hand (2 levels), and handgrip
(5 levels) as factors, was performed on the muscular effort data
1665
(in kilograms). The only significant main effects were for hand
(F1,26⫽6.76, P⬍.015, partial ␩2⫽.21), and for handgrip
(F2.3,59.3⫽551.7, P⬍.001, partial ␩2⫽.96), which were not of
interest in the current study. The interaction, handgrip by
perceptual status was also significant (F8,59.4⫽3.18, P⬍.005,
partial ␩2⫽.20); however, when the appropriate Bonferroni
adjustment for family-wise error was applied, none of the
paired comparisons among the 3 groups proved statistically
significant for any handgrip condition. We therefore conclude
that joint and motor capabilities did not differ among the 3
groups in the current study.
Cutaneous Force Sensitivity and Cutaneous
Spatial Resolution
A mixed-factor ANOVA was performed on the force sensitivity thresholds. The 2 within-subjects factors included hand
site (3 levels: fingertip [mean of thumb, index, little fingers],
proximal phalanx [mean of index and little fingers], and palm)
and hand (2 levels: left, right). The between-subjects factor was
perceptual status (3 levels: diabetic blind, nondiabetic blind,
sighted controls groups). The dependent variable was the mean
force threshold (in grams), averaged across fingers. A second
mixed-factor ANOVA was performed on the 3 tests of cutaneous spatial resolution. Thus, in addition to the same 3 factors
included in the force ANOVA, we added a fourth withinsubjects factor, test (3 levels: static 2PT, moving 2PT, point
localization). The dependent variable was spatial threshold (in
millimeters), averaged across the fingers tested at each position. To adjust for family-wise error, we performed a Bonferroni adjustment on all paired-comparison tests of mean differences.
The results for force sensitivity and for the 3 tests of spatial
resolution are presented in table 1. Only statistically significant
effects are included. The diabetic blind group showed significantly higher force thresholds than either nondiabetic blind or
sighted control groups, which were not significantly different.
This impairment was evident at all 3 hand sites. The effect of
hand site showed the typical distal-to-proximal gradient, with
force sensitivity being highest on the fingertip, next on the
proximal, phalange, and lowest on the palm. The perceptual
status by hand site interaction term further revealed that the
distal-to-proximal gradient in sensitivity was most distinct for
the diabetic blind group. Finally, in keeping with Weinstein’s
earlier results,28 the left hand was more sensitive to force than
the right hand.
As with force sensitivity, the spatial-resolution capacity of
the diabetic blind group was significantly lower than that of
either the nondiabetic blind or blindfolded sighted groups,
which were not significantly different. It is potentially interesting that there was also a consistent but nonsignificant trend in
both the force-sensitivity and spatial-resolution data for nondiabetic blind controls to be more spatially acute than blindfolded sighted controls. In keeping with other studies,13 there
was also a distinct distal-to-proximal spatial gradient from
fingertip (highest) to palm (lowest). A significant interaction
between hand site and perceptual status indicated that although
the spatial-gradient main effect was clearly evident in each
group, the spatial thresholds (inverse of spatial resolution) on
the proximal phalanx, and likewise on the palm, were at both
sites equivalent for the diabetic blind and sighted subjects and
worse than for the nondiabetic blind subjects. Only on the
finger pad was the spatial threshold for the diabetic blind group
higher than for the blindfolded sighted control (or nondiabetic
blind) group. Although the patterns just described were very
similar across all 3 spatial tasks, there were 2 additional effects
involving task. The main effect of task showed that spatial
Arch Phys Med Rehabil Vol 88, December 2007
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TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
Table 1: Statistical Results of the ANOVAs for Cutaneous Force Sensitivity and Spatial Resolution
Task
Force sensitivity
Spatial resolution (inverse of threshold)
Significant Factor Effects
Hand site
F2,52⫽13.02, P⬍.001, partial ␩2⫽.33
Perceptual status
F2,26⫽16.46, P⬍.001, partial ␩2⫽.56
Hand site by perceptual status
F4,52⫽4.17, P⬍.005, partial ␩2⫽.24
Hand
F1,26⫽25.74, P⬍.001, partial ␩2⫽.50
Task
F2,48⫽79.47, P⬍.001, partial ␩2⫽.77
Position
F1.6,48⫽331.41, P⬍.001, partial ␩2⫽.93
Task by hand site
F2.6,62.9⫽27.95, P⬍.001, partial ␩2⫽.54
Perceptual status
F2,24⫽10.45, P⬍.001, partial ␩2⫽.47
Perceptual status by hand site
F4,48⫽8.08, P⬍.001, partial ␩2⫽.40
Description of Significant Effects
Distal-proximal sensitivity gradient
For all hand sites, DB more sensitive
than NDB-B and SIG, which were
not significantly different
Distal-to-proximal gradient most clear
for DB
Left more sensitive than right
Point localization ⬎ moving 2PT ⬎
static 2PT
Distal-to-proximal spatial gradient
Main effect of task clearest on
proximal phalanx and palm
DB ⬍ (NDB-B ⫽ SIG)
Clear distal-to-proximal spatial
gradient effects for each group
DB ⬍ SIG on finger pad
DB ⫽ SIG on proximal phalanx and
palm
Consistent tendency with respect to
spatial resolution: NDB-B ⬎ SIG at
all hand sites
Abbreviations: DB, diabetic blind group; NDB-B, nondiabetic blind control group; SIG, blindfolded sighted control group.
resolution varied from highest to lowest in the following order:
point localization, moving 2PT, and static 2PT. A significant
interaction between task and hand site further revealed that the
spatial-gradient effect was very evident for all 3 tasks, with the
size of the effect decreasing slightly from static 2PT to moving
2PT to point localization. Also in keeping with Weinstein,28
each task showed equivalent spatial resolution regardless of
hand. Figure 1 presents the mean finger-pad thresholds for both
cutaneous force sensitivity (left hand, right hand) and for
cutaneous spatial resolution (by separate test) for diabetic
blind, nondiabetic blind, and sighted (blindfolded) groups.
Only the finger pad is represented graphically because subclinical impairments in both force sensitivity and spatial resolution
occurred uniformly in the diabetic blind group at this most
distal hand site.
Haptic Category Scaling of the Physical Magnitude of
Object Dimension
The psychophysical tasks performed by category scaling
restrict judgments to the highest and lowest numeric values that
Fig 1. Mean cutaneous thresholds for force sensitivity and spatial resolution by perceptual status on the finger pad. Note that thresholds are
inversely related to force sensitivity and spatial resolution.
Arch Phys Med Rehabil Vol 88, December 2007
TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
1667
lower cutaneous thresholds were associated with steeper rates
of growth for texture reflecting finer texture differentiation.
The specific correlation between the slope of the psychophysical function for texture with static 2PT threshold was ⫺.40
(P⬍.05), with moving 2PT threshold it was ⫺.49 (P⬍.05),
with point localization it was ⫺.38 (P⬍.05), and with force
threshold it was ⫺.07 (P⬎.05).
As mentioned earlier, it is important to emphasize that
although diabetic blind subjects had higher somatosensory
thresholds for all 4 cutaneous tests in our study, only the
spatial-resolution tests showed a direct relation with a perceptual dimension, namely, surface texture. Although force and
other passive sensory tests (eg, vibration, thermal) allow the
detection of peripheral neuropathies, to our knowledge they
have never been used before as tools for predicting performance on haptic perception tasks.
Fig 2. Psychophysical functions for category scaling of texture.
can be assigned to the physical stimulus. In the current study,
as subjects chose not to use either extreme value, we fitted
linear functions to the mean category values (perceived magnitude) as a function of the physical stimulus magnitudes for
each subject and each dimension. The slope was then used as
a relative measure of rate of growth of sensation. The linear fits
to the data were excellent (R2⬎.90), with the exception of 2
subjects in the diabetic blind group (R2⫽.66, R2⫽.73).
A 2-factor mixed ANOVA was performed on the slope data.
The within-subject factor was dimension (4 levels) and the
between-subject factor was perceptual status (3 levels). The
only significant main effect was dimension (F1.2,26⫽2261.82,
P⬍.001, partial ␩2⫽.99). This was to be expected as the
perceptual ranges were only approximately equated across
dimensions. Moreover, relative slope values will vary depending on the units of measure adopted. In any event, the effect of
dimension per se was not relevant to the goal of this study, and
will not be addressed further. Paired comparisons among the 3
perceptual status means were performed within each dimension
with the appropriate Bonferroni adjustment for family-wise
error. For texture, the slope for the diabetic blind was less steep
than for either the nondiabetic blind or blindfolded sighted
controls, which were not statistically different from each other
(fig 2). The mean slope for volume (cube) for the blindfolded
sighted group was marginally but statistically steeper than that
for the nondiabetic blind group (Pⱕ.05), an unexpected result
that we are currently unable to explain.
Correlations Between Cutaneous Sensitivity and
Haptically Perceived Dimension Magnitude
Bernbaum et al9 suggested that sensory thresholds may be
related to the performance of suprathreshold perceptual and
motor tasks, namely, Braille reading. Tremblay et al22,23 also
showed a correlation between manual dexterity and spatial
acuity. In these studies, researchers found an inverse relation
between somatosensory thresholds for both spatial acuity and
dexterity and Braille reading performance. To evaluate the
relation between threshold and suprathreshold performance in
the current study, we determined correlations between measures of cutaneous thresholds and slopes of the psychophysical
functions for the category-rating tasks. The only significant
differences were between each of the 3 cutaneous spatial
thresholds and the slope of the psychophysical function for
texture. The spatial thresholds were inversely correlated with
the slope of the psychophysical function for texture; that is,
Manual Dexterity: Moberg Pick-up Test
Errors. Because there were only 3 naming errors in total,
we did not analyze the error data.
Response times. A mixed 2-factor ANOVA was performed on the response times (in seconds), with hand (2 levels)
and perceptual status (3 levels) as factors. The main effect of
hand was significant (F1,25⫽13.52, P⬍.001, partial ␩2⫽.35):
the right hand was faster than the left hand. This result was
expected because all subjects were right-handed. The main
effect of perceptual status was also significant (F2,25⫽5.10,
P⬍.05, partial ␩2⫽.29). Pairwise t tests were performed on the
differences between perceptual status (means separately for
right and left hands). The only significant differences were
between diabetic blind and nondiabetic blind groups for both
right and left hands. The diabetic blind group was significantly
slower than the nondiabetic blind group for both hands (right
hand: t17⫽2.83, P⬍.015; left hand: t17⫽2.84, P⬍.015), and
tended to be slower than the blindfolded sighted group, again
for both hands (right hand: t16⫽1.36, P⫽.19; left hand:
t16⫽1.56, P⬍.14), as shown in figure 3. The nondiabetic blind
and sighted control groups were statistically equivalent.
Manual Dexterity: MRMT
The mean response time (in seconds) for each subject was
calculated by averaging across the 3 trials. A 2-factor mixed
ANOVA was performed with subscale (3 levels) and perceptual status (3 levels) as factors. It showed significant main
effects of subscale (F2,52⫽17.58, P⬍.001, partial ␩2⫽.40) and
perceptual status (F2,26⫽4.15, P⬍.05, partial ␩2⫽.24 ), with no
significant effect due to their interaction (see fig 4). Not surprisingly, in accord with standardized results, the bimanual
turning subscale was performed in less time by all groups
Fig 3. Moberg Pick-up Test performance time by hand and perceptual status.
Arch Phys Med Rehabil Vol 88, December 2007
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TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
Fig 4. Mean MRMT performance time by subtest and perceptual
status.
Fig 5. Mean response time for haptic 3-dimensional object recognition for diagnostic properties by perceptual status.
(mean, 89.74; 95% confidence interval, 79.59⫺99.90), with no
significant differences between the unimanual displacement
subscales.
The diabetic blind group tended to be slower than both
control groups on all 3 subscale tests, although only the differences with the nondiabetic blind controls proved statistically
significant using the conservative Scheffé test for mean paired
comparisons (diabetic blind vs nondiabetic blind, P⬍.05; diabetic blind vs sighted, P⬎.05; nondiabetic blind vs sighted,
P⬎.05).
Haptic 3-Dimensional Common-Object Identification
A 2-factor mixed design was used with the between-subject
factor being perceptual status (3 levels) and the within-subject
factor being diagnostic property (6 levels). Subjects in each
group identified all objects in each diagnostic property category.
Accuracy. Categorization accuracy was very high for all
subjects and objects. A total of 26 objects were categorized
with a mean accuracy of more than 90%. Only 6 of these were
recognized with 100% accuracy. In addition, 3 others were
recognized with over 80% accuracy, and one (empty coffee
can) with 75% accuracy. Only 1 object, the piece of corduroy
(texture– diagnostic), showed significant differences between
groups. More specifically, it was recognized by 100% of the
subjects in the 2 control groups and by only 66% of the subjects
in the diabetic blind group. Differences in mean accuracy
between groups were evaluated using the Kruskal-Wallis test.
There were no statistical differences (␹22 test⫽1.85, P⫽.40),
although the diabetic blind group tended to be slightly less
accurate (mean ⫾ standard error of the mean, 90.0%⫾2.3%)
than the nondiabetic blind (mean, 95.0%⫾1.4%) and the blind-
folded sighted (mean, 94.8%⫾1.2%) control groups. Mean
recognition accuracy across subjects was 93%. Only 2 of the
subjects were less accurate (ie, 79%), and both were diabetic
blind subjects. Only 4 subjects (1 nondiabetic blind, 3 sighted
subjects) scored 100% accuracy. We conclude that there was
no ceiling effect, whether subject or object was used as the unit
of observation.
Response time. To address the effects on response time,
we performed a 2-factor mixed ANOVA, with diagnostic property (6 levels) and perceptual status (3) as within- and betweensubject factors, respectively. Results show a significant main
effect of perceptual status (F2,26⫽4.96, P⬍.05, partial ␩2⫽.28),
with the diabetic blind being significantly slower than nondiabetic blind and blindfolded sighted controls (Scheffé test
mean differences: diabetic blind vs nondiabetic blind, 1.28;
P⬍.05; diabetic blind vs blindfolded sighted, 1.33; P⬍.05).
The 2-way interaction term was not statistically significant.
The mean response time for each diagnostic property by perceptual status is shown in figure 5.
DISCUSSION
The current study offers a more comprehensive assessment
than earlier research of the extent to which manual touch is
impaired by diabetes, particularly in diabetic blind subjects for
whom the sense of touch is especially critical during rehabilitation and re-education. The battery of tests broadly evaluated
manual function in terms of both tactile and haptic sensing. As
previously documented with sighted diabetics,3,14 the current
results highlight significantly higher cutaneous thresholds for
diabetic blind adults that were detectable prior to the appear-
Table 2: Impaired Hand Function in Diabetic Late-Blind Adults
Type of Hand Function
Cutaneous
Musculoskeletal
Motor dexterity
Haptic
Assessment Test
Passive sensibility
Force
Two-point threshold (static)
Two-point threshold (moving)
Localization
Joint mobility and muscular strength
Moberg Pick-up Test (fine)
MRMT (coarse)
Category rating of magnitude of object properties
Classification of common objects
Arch Phys Med Rehabil Vol 88, December 2007
Functional Disturbance
High (all 3 hand positions)
High (fingertip)
High (fingertip)
High (fingertip)
None
High
High
High for texture; none for weight or volume
High for duration of exploration
High for texture-diagnostic objects
None for other property-diagnostic objects
(temperature, hardness, weight, form, or size)
TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
ance of clinical symptoms of peripheral neuropathy. Table 2
summarizes our major findings. Impairments in both force
sensitivity and spatial resolution were consistently observed on
the finger pad, the most distal hand site; although force sensitivity was also impaired on the 2 more proximal sites, spatial
resolution remained unaffected. Finally, we noted a nonsignificant but highly consistent tendency for the nondiabetic blind
controls to be more sensitive to force (finger pad, proximal
phalanx) and more spatially acute than the blindfolded sighted
controls. This noteworthy tendency may be attributed to increased manual experience in the nondiabetic blind controls.
With a larger sample size, this sensory enhancement effect of
experience may have become statistically significant.
Given the specific contribution of cutaneous (cf kinesthetic)
inputs to texture perception,31-34 our results suggest that such
cutaneous disturbances in diabetic blind people have their main
functional impact on the capacity to differentiate surface textures. In addition, our study also helps to explain previous
experimental findings of an association between impaired cutaneous sensitivity thresholds and poor Braille reading. In
terms of our current scientific knowledge about the sense of
touch, tasks involving texture and other microdot patterns (eg,
Braille) rely on the fundamental integrity of the cutaneous, as
opposed to the haptic, subsystem.35,36
The absence of differences in joint mobility and muscular
strength were in keeping with the fact that diabetic blind
persons showed no deficits in assessing the other object properties tested, including weight and volume, all of which are
primarily dependent on “dynamic touch,” a subsystem that
specifically requires intact kinesthesis.37 We conclude that at
least at this stage of the disease, the percepts of these fundamental object properties are unaffected by diabetic complications.
As we have seen, diabetic blind subjects did not significantly
differ from control groups in muscular strength or joint function that may produce motor difficulties in this at-risk population. Therefore, the motor disturbances documented by the 2
tests of dexterity (despite the absence of standardized norms for
the blind) would seem to be caused by reduced cutaneous hand
function in the diabetic blind group.
The sensory deficits found in diabetic blind subjects did not
notably affect the accuracy of multi-attribute common-object
classification, because all groups performed very well (ie,
⬎90%). Although it is possible that such high accuracy was the
result of there being only 30 objects in the task, we believe it
is unlikely because mean identification accuracy in the original
study by Lederman and Klatzky26 was close to 100% when 100
common objects were presented. We propose rather that the
high accuracy scores may indicate that relatively coarse variation in object features is sufficient for the constrained classification of common objects. In keeping with their impaired
motor dexterity, the diabetic blind were significantly slower
than the 2 control groups, revealing the impact of functional
1669
cutaneous impairments on grasping and manipulation. Two
studies lend support to this interpretation. Westling and Johansson38 showed impairments in fine motor control of the fingers
when the normal hand was anesthetized to eliminate normal
cutaneous inputs. Jessel39 documented significant impairments
in cutaneous sensitivity and motor dexterity in older subjects,
relative to younger subjects. Although the former were statistically slower than the latter, as in the current study, they
showed relatively very little deficit in the accuracy with which
they haptically identified common objects.
Study Limitations
In this study, the nondiabetic blind and diabetic blind groups
differed substantially in their tactile experience (19.5y vs 8y in
duration of blindness, respectively). It is possible that the
difference in tactile experience due to blindness might have
contributed to the observed differences in performance. Nevertheless, any such effects were at best small, relative to the
substantial effects documented in this study due to subclinical
peripheral neuropathy in the blind diabetic group. Our reasoning is based on the fact that this variable had no statistically
significant effects on the relative performance of nondiabetic
blind versus sighted blindfolded subjects, where the difference
in tactile experience was even greater. As mentioned above, we
suggest that the small but consistent improvement due to tactile
experience may be confirmed in future with use of larger
sample sizes.
CONCLUSIONS
The current study used a comprehensive battery of diagnostic tests to comprehensively assess the tactual function of
diabetic late-blind subjects, a group at risk for peripheral neuropathy that may pose a special challenge for blindness rehabilitation professionals.11 In keeping with our hypotheses, we
found that the diabetic blind were mainly impaired in tactile
sensing (force sensitivity and spatial resolution), and in the
haptic categorization of surface textures and haptic identification of common objects for which texture was the most diagnostic property. We conclude that only perceptual and motor
tasks for which cutaneous (cf kinesthetic) information is important were impaired, relative to nondiabetic blind and blindfolded sighted control groups. Performance on perceptual tasks
that required intact kinesthetic information was unaffected.
Clinical Implications
Understanding the nature of the touch deficits likely sustained by diabetic late-blind persons who are at risk for peripheral neuropathy is particularly important to rehabilitation professionals who must develop appropriate rehabilitation and
re-education programs for this subpopulation of diabetics.
Acknowledgment: We thank Cheryl Hamilton, MA, for her assistance in preparing the revised manuscript for publication.
APPENDIX 1: DESCRIPTION OF PARTICIPANTS
The sample of the study is formed by an experimental group
and 2 control groups. A total of 9 blind subjects with diabetes
mellitus, and diagnosed with diabetic retinopathy constituted
the experimental group. This is a risk population for peripheral
neuropathy. All subjects belong to the special center for General and Visual Rehabilitation of the Spanish National Organization for the Blind.
We assume that confronting the difficulties for an early
diagnosis of peripheral diabetic neuropathy, and given the
appearance of signs and symptoms in subclinic forms, our tasks
may function for early detection and diagnosis of functional
disturbances. Therefore, we do not require the pathology diagnosis in order to include the diabetics in the experimental
sample. Table A1.1 shows the participants’ description.
Arch Phys Med Rehabil Vol 88, December 2007
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TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
APPENDIX 1: DESCRIPTION OF PARTICIPANTS (cont’d)
Table A1.1: Blind Diabetic Group
N
Age (y)
Diabetes
1
2
3
4
5
6
7
8
9
Mean
72
72
68
55
49
48
43
33
27
51.8
Type I
Type I
Type II
Type I
Type II
Type I
Type I
Type I
Type I
Duration of
Diabetes (y)
32
5
49
30
5*
14
41
10
18
22.5
Education
Visual
Deficiency
Duration of
Blindness (y)
Cognitive
Abilities
Hand
Dominance
None
Primary
University
None
Primary
University
High school
University
High school
VI, DR
VI, DR
VI, DR
TB, DR
TB, DR
VI, DR
VI, DR
TB, DR
VI, DR
10
3
16
15
5
1
16
2
3
8
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Right
Right
Right
Right
Right
Right
Right
Right
Right
Abbreviations: DR, diabetic retinopathy; TB, totally blind; VI, visually impaired, with no functional vision.
*The detection of diabetes was coincident with blindness.
A total of 10 totally blind subjects without diabetes or
any type of neuropathy formed the first control group.
All subjects belong to the Special Center for General
and Visual Rehabilitation of the Spanish National Organization for the Blind. Table A1.2 describes the participants.
Table A1.2: Blind Control Group
N
Age (y)
Education
Visual
Deficiency
Duration of
Blindness (y)
Cognitive
Abilities
Hand
Dominance
1
2
3
4
5
6
7
8
9
10
Mean
23
54
41
45
29
39
56
40
51
59
43.7
Primary
Primary
University
University
Professional school
High school
High school
Primary
High school
High school
VI, CP
VI, M
TB, GL
TB, PR
TB, HI
TB, GL
TB, RD
TB, PR
TB, PR
TB, ONP
2
10
34
6
11
21
8
10
41
51
19.5
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Right
Right
Right
Right
Right
Right
Right
Right
Right
Right
Other Information
Braille teacher
Abbreviations: CP, chronic panuveitis; GL, glaucoma; HI, head injury; M, myopia; ONP, optic nerve pathology; PR, pigmentary retinitis; RD,
retinal degeneration.
Table A1.3 describes the 10 sighted controls.
Table A1.3: Sighted Control Group
N
Age (y)
Education
Cognitive Abilities
Hand Dominance
1
2
3
4
5
6
7
8
9
10
Mean
80
58
67
56
57
31
41
41
42
28
50
None
Primary
High school
High school
University
University
University
University
University
University
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Right
Right
Right
Right
Right
Right
Right
Right
Right
Right
Arch Phys Med Rehabil Vol 88, December 2007
Other Information
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TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso
APPENDIX 2: COMMON OBJECTS USED IN THE CONSTRAINED HAPTIC IDENTIFICATION TASK
Diagnostic Property
Object
Category Level
Correct Answer
Dessert fork
Woman’s hand watch
House key
Hotel soap
Shirt button
Subordinate
Subordinate
Subordinate
Subordinate
Subordinate
Yes
No
Yes
Yes
No
Wine glass
Can
Spaghetti
Sunflower seed
Paper clip
Subordinate
Basic
Subordinate
Subordinate
Subordinate
Yes
No
Yes
No
Yes
Fine sandpaper
Plush towel
Fine corduroy swatch
Pencil rubber
Wood pegs
Subordinate
Subordinate
Subordinate
Subordinate
Subordinate
Yes
No
Yes
No
Yes
Metallic clip
Metallic pencil
Sharpener
Metallic can
Flask
Metallic glasses
Subordinate
Subordinate
Subordinate
Subordinate
Basic
Subordinate
Yes
No
Yes
No
Yes
No
Throwaway shaver
Newspaper
Plastic pencil sharpener
Coffee bottle
Book
Subordinate
Basic
Subordinate
Subordinate
Basic
Yes
No
Yes
No
Yes
Paper table cloth
Hard-cover book
Match box
Toothpaste tube
Dry dough
Subordinate
Subordinate
Subordinate
Subordinate
Subordinate
Yes
Yes
No
Yes
No
Size
Form
Texture
Temperature
Weight
Hardness
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Supplier
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11801.