IT IS WELL KNOWN THAT the retinopathy caused by

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1 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: 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 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. BFF , HUM 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, susan.lederman@queensu.ca /07/ $32.00/0 doi: /j.apmr IT IS WELL KNOWN THAT the retinopathy caused by diabetes mellitus is one of the main causes of adult blindness. 1,2 Professionals who deal with blind diabetic adults usually 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 reading 9-11 ) 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

2 TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso 1663 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 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 effort 21 for 5 different handgrips: fist, lateral, thumb-index, thumb-index/middle, and thumb-little. Subjects were required to press 5 hand tenders a 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 recognition 12 ). Motor dexterity. Although we documented no significant differences in either joint mobility or muscular strength among our 3 groups, several studies with diabetic 10 and nondiabetic populations 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 Test 25 evaluates fine motor dexterity for hand rehabilitation of patients who have undergone hand surgery. It consists of a square plastic box, with dimensions

3 1664 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, ). 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 120cm 3 in increments of 8cm 3, 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 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

4 TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso 1665 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 (in kilograms). The only significant main effects were for hand (F 1, , P.015, partial 2.21), and for handgrip (F 2.3, , P.001, partial 2.96), which were not of interest in the current study. The interaction, handgrip by perceptual status was also significant (F 8, , 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

5 1666 TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso Table 1: Statistical Results of the ANOVAs for Cutaneous Force Sensitivity and Spatial Resolution Task Significant Factor Effects Description of Significant Effects Force sensitivity Hand site Distal-proximal sensitivity gradient F 2, , P.001, partial 2.33 Perceptual status F 2, , P.001, partial 2.56 For all hand sites, DB more sensitive than NDB-B and SIG, which were not significantly different Hand site by perceptual status F 4, , P.005, partial 2.24 Distal-to-proximal gradient most clear for DB Hand Left more sensitive than right F 1, , P.001, partial 2.50 Spatial resolution (inverse of threshold) Task F 2, , P.001, partial 2.77 Point localization moving 2PT static 2PT Position Distal-to-proximal spatial gradient F 1.6, , P.001, partial 2.93 Task by hand site F 2.6, , P.001, partial 2.54 Main effect of task clearest on proximal phalanx and palm Perceptual status F 2, , P.001, partial 2.47 DB (NDB-B SIG) Perceptual status by hand site F 4, , P.001, partial 2.40 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.

6 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 (R 2.90), with the exception of 2 subjects in the diabetic blind group (R 2.66, R 2.73). 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 (F 1.2, , 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 (P.05), an unexpected result that we are currently unable to explain. Correlations Between Cutaneous Sensitivity and Haptically Perceived Dimension Magnitude Bernbaum et al 9 suggested that sensory thresholds may be related to the performance of suprathreshold perceptual and motor tasks, namely, Braille reading. Tremblay et al 22,23 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 (F 1, , 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 (F 2, , 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: t , P.015; left hand: t , P.015), and tended to be slower than the blindfolded sighted group, again for both hands (right hand: t , P.19; left hand: t , 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 (F 2, , P.001, partial 2.40) and perceptual status (F 2, , 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.

7 1668 TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso Fig 4. Mean MRMT performance time by subtest and perceptual status. (mean, 89.74; 95% confidence interval, ), 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). Fig 5. Mean response time for haptic 3-dimensional object recognition for diagnostic properties by perceptual status. 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 ( 2 2 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 blindfolded 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 (F 2, , 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 Assessment Test Functional Disturbance Cutaneous Passive sensibility Force High (all 3 hand positions) Two-point threshold (static) High (fingertip) Two-point threshold (moving) High (fingertip) Localization High (fingertip) Musculoskeletal Joint mobility and muscular strength None Motor dexterity Moberg Pick-up Test (fine) High MRMT (coarse) High Haptic Category rating of magnitude of object properties High for texture; none for weight or volume Classification of common objects High for duration of exploration High for texture-diagnostic objects None for other property-diagnostic objects (temperature, hardness, weight, form, or size)

8 TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso 1669 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, 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 Klatzky 26 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 cutaneous impairments on grasping and manipulation. Two studies lend support to this interpretation. Westling and Johansson 38 showed impairments in fine motor control of the fingers when the normal hand was anesthetized to eliminate normal cutaneous inputs. Jessel 39 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.

9 1670 TOUCH DEFICITS IN THE DIABETIC BLIND, Travieso APPENDIX 1: DESCRIPTION OF PARTICIPANTS (cont d) Table A1.1: Blind Diabetic Group N Age (y) Diabetes Duration of Diabetes (y) Education Visual Deficiency Duration of Blindness (y) Cognitive Abilities Hand Dominance 1 72 Type I 32 None VI, DR 10 Normal Right 2 72 Type I 5 Primary VI, DR 3 Normal Right 3 68 Type II 49 University VI, DR 16 Normal Right 4 55 Type I 30 None TB, DR 15 Normal Right 5 49 Type II 5* Primary TB, DR 5 Normal Right 6 48 Type I 14 University VI, DR 1 Normal Right 7 43 Type I 41 High school VI, DR 16 Normal Right 8 33 Type I 10 University TB, DR 2 Normal Right 9 27 Type I 18 High school VI, DR 3 Normal Right Mean 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 Other Information 1 23 Primary VI, CP 2 Normal Right 2 54 Primary VI, M 10 Normal Right 3 41 University TB, GL 34 Normal Right Braille teacher 4 45 University TB, PR 6 Normal Right 5 29 Professional school TB, HI 11 Normal Right 6 39 High school TB, GL 21 Normal Right 7 56 High school TB, RD 8 Normal Right 8 40 Primary TB, PR 10 Normal Right 9 51 High school TB, PR 41 Normal Right High school TB, ONP 51 Normal Right Mean 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 Other Information 1 80 None Normal Right 2 58 Primary Normal Right 3 67 High school Normal Right 4 56 High school Normal Right 5 57 University Normal Right 6 31 University Normal Right 7 41 University Normal Right 8 41 University Normal Right 9 42 University Normal Right University Normal Right Mean 50