Touch in aging

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Francois Tremblay and Sabah Master (2015), Scholarpedia, 10(2):9935. doi:10.4249/scholarpedia.9935 revision #149559 [link to/cite this article]
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Curator: Francois Tremblay

While hearing loss and decreased eyesight are things we all expect with aging, we are less aware of the changes that also affect other sensory systems. For instance, people often experience substantial decline in their ability to detect and discriminate touch stimuli as they age and yet, these changes often go unnoticed for years. Touch in Aging provides an overview of results from past and current studies that have examined the impact of age on tactile performance in human observers. We also address briefly the reasons as to why some tactile abilities are more affected than others by age and why tactile experience might be an important factor in modulating age effects in senior individuals.

Contents

Changes in tactile performance with age

Given its primary importance in the sense of touch, this section will focus on the changes affecting the sensory function of the hand. In addition, following the terminology introduced by Jones and Lederman (2006) to distinguish between passive and active modes of touch, we will first address changes affecting tactile sensing abilities, i.e. when stimuli are applied to the passive hand. This mode of sensing allows for control of stimulus delivery and thus provides an ideal context to examine changes affecting the hand’s sensitivity and spatial resolution. Afterwards, we will turn our attention to changes affecting haptic sensing abilities, i.e. when the hand is actively engaged in tactile exploration of objects’ material and spatial properties.

Changes in touch sensitivity and spatial resolution with age

One of the early noticeable signs of aging in sensory perceptual systems is the decline of various forms of sensitivity, i.e. a decrease in the ability to detect near-threshold stimuli. Two forms of sensitivity that have been particularly investigated in the context of aging are pressure sensitivity and vibrotactile detection.

Pressure sensitivity

The ability to detect light pressure is usually assessed using von Frey filaments of different diameters, such as those introduced by Semmes and Weinstein (Weinstein 1993). Each filament is calibrated to bend to a specific buckling force which translates into pressure in g/mm2. For instance, the 2.83 filament, which is often taken as the norm for screening changes in pressure detection, corresponds to 0.07 g of force (Bell-Krotoski, Weinstein et al. 1993, Bell-Krotoski, Fess et al. 1995). In healthy seniors, pressure sensitivity in the hand, as assessed with filaments, is usually decreased relative to norms (Desrosiers, Hebert et al. 1999) or when compared to a younger population (Bruce and Sinclair 1980, Tremblay, Mireault et al. 2005). There is also a general consensus that these changes become more noticeable during the sixth decade and then, tend to increase as people advance in age (Thornbury and Mistretta 1981, Bowden and McNulty 2013). The degree of impaired sensitivity, however, varies considerably between individuals. The importance of this variability was highlighted in a report by Thornbury and Mistretta (1981), who noted that despite the fact that most seniors exhibited higher detection thresholds after 60 years, a substantial proportion (~ 40%) still retain a sensitivity comparable to that of younger groups of participants. In this study, the mean detection threshold at the fingertip was 2.74 in the group of seniors aged over 60 years, whereas it was 2.18 in the participants aged less than 30 years, which translates into a 3-fold increase with age when expressed in mg of force. Using a similar methodological approach (i.e., forced choice paradigm), Tremblay, Mireault et al. (2005) reached a similar conclusion with regard to both individual variability among seniors and the relative increase with age in detection threshold for light pressure at the fingertip (young, 2.50, senior 3.21).

Vibrotactile sensitivity

Much like pressure, sensitivity to vibration also declines with age. In this regard, the work of Verrillo and colleagues (Verrillo 1979, Verrillo 1980) has been particularly enlightening. From the early 80s to mid-90s, these investigators ran a series of experiments examining vibrotactile sensitivity in relation to age linked with factors such as frequency, duration of stimulation and contact area. In general, these studies have revealed that sensitivity to vibration starts to decline substantially during the sixth decade and then deteriorates further with more advancing age (Gescheider 1965). In addition, the loss in sensitivity was far more pronounced for detection of high frequencies (e.g. 250-300 Hz) than for low frequencies (e.g. 35-40 Hz) (Verrillo 1979, Verrillo 1980, Gescheider, Edwards et al. 1996). For example, detection thresholds for 300 Hz stimuli increased by 30 dB over the age range 10 to 89 years (Gescheider, Edwards et al. 1996). Along the same line, the perceived intensity of supra-threshold vibratory stimuli (250 Hz) was greatly decreased with age, with a 16 dB loss between 20 and 60 years of age (Verrillo, Bolanowski et al. 2002). Collectively, these observations (e.g., decreased sensitivity for high frequencies) were interpreted as evidence for an age-related sensory loss particularly in the Pacinian channel (i.e., Pacini receptors). As for the Non-Pacinian channel (e.g., Meissner receptors) mediating detection of low frequencies, although the loss seems less pronounced than in the PC channel, it is still significant with age (Gescheider et al. 1994). Subsequent works have largely confirmed the observations of Verrillo and colleagues as to the primary importance of age in influencing vibrotactile sensitivity for both low and high frequencies (Goble, Collins et al. 1996, Stevens, Cruz et al. 1998, Lin, Hsieh et al. 2005, Bhattacherjee et al. 2010).

Spatial acuity

Humans possess a very refined ability to discriminate spatial details, especially at the fingertip, where the high density innervation allows for fine spatial resolution. Various tasks and stimuli have been employed to examine spatial acuity in the resting hand, including “the classical” two-point limen test. Although still widely used clinically, the two-point test and its variants remain problematic for their interpretation is blurred by the presence of intensive cues affecting the perception of single vs. double point stimuli (Johnson and Persinger 1994). In fact, careful investigations by Johnson and colleagues have shown that observers can actually discriminate between single and double-point stimuli even when there is no physical separation between the two probes, thus invalidating the two-point limen as a test for spatial acuity (for more recent development on this issue see Tong, Mao et al. 2013). Instead, after the seminal work of Johnson and colleagues (Johnson and Lamb 1981), investigators turn to grooves and gaps as spatial stimuli to test spatial acuity. With such stimuli, the limit of spatial resolution at the fingertip in young adults has been shown to be ~1 mm (Van Boven, Johnson et al. 1991, Van Boven and Johnson 1994, Sathian and Zangaladze 1996), i.e. close to the theoretical limit imposed by the estimated innervation density in this area (Johansson and Vallbo 1979). As expected, with age there is marked decline in spatial resolution. In an elegant series of experiments led in the 90s, Stevens and colleagues (Stevens 1992, Stevens, Cruz et al. 1995, Stevens and Patterson 1995, Stevens and Choo 1996, Stevens and Cruz 1996) examined age-related changes in spatial acuity across different body areas. These experiments showed that age-related alterations in spatial acuity were ubiquitous across the body surface, although the decline was more pronounced in the distal extremities. For instance, changes in resolution thresholds with advancing age averaged 400% in the foot area whereas it averaged 130% at the fingertip. The fact that spatial acuity was particularly affected at the fingers was further corroborated by Tremblay and colleagues (Tremblay, Backman et al. 2000, Tremblay, Wong et al. 2003) who used the grating orientation task developed by Van Boven and colleagues (Van Boven, Johnson et al. 1991) to assess spatial resolution threshold. Their observations revealed a substantial decline in acuity with age, older adults exhibiting almost a threefold increase in grating resolution threshold (mean 2.7 mm) at the index finger. In addition, the decline in spatial acuity observed in seniors correlated strongly with decreased manual dexterity, suggesting a link between changes in tactile sensation at the fingertip and declining manual dexterity with advancing age. Subsequent investigations by Goldreich and colleagues (2003, Wong et al. 2011) examining grating orientation acuity using a precision-controlled stimulus system in large groups of sighted as well as blind participants showed significant age-related decline among both groups. Interestingly, while at any given age blind participants had on average better performance, spatial acuity in the two groups declined at an equal rate with age (see Fig. 4 of Goldreich and Kanics, 2003), lending support to the hypothesis that the age-related decline in spatial acuity is due to loss of peripheral receptors (e.g. SA1 afferents or Merkel cells, see below). Still, it seems clear that blind people somehow process tactile input more effectively than sighted people as their performance always outweighed that of their sighted peers.

Haptic sensing

While there are numerous reports describing age-related changes in tactile sensing, the range of observations for haptic sensing is comparatively smaller. In the next section we will highlight the results of experiments examining how age affects haptic performance in recognizing two-dimensional (2-D) patterns, shapes and texture by touch. We will conclude by examining performance for three-dimensional (3-D) objects.

Tactile recognition of 2-D patterns

Recognition of 2D patterns is a common task that we do almost every day (e.g., determine which button to press using patterns imprinted on your car’s key). Yet, pattern recognition is an inherently difficult task for its performance relies on the integration of sparse inputs generated from multiple contacts as the finger explores the contour (Lederman and Klatzky 1997). In spite of this difficulty, young adults can achieve very high levels of accuracy even after minimal training (Loomis 1982, Vega-Bermudez, Johnson et al. 1991, Manning and Tremblay 2006). This level of performance, however, is greatly compromised with age. For instance, Manning and Tremblay (2006) found a 38% decline in performance when comparing young and older adults’ ability to recognize Roman letters by haptic exploration (mean hit rate, 88 ± 8% vs. 55 ± 18%, respectively). Interestingly, individual variations in letter recognition were highly correlated with spatial acuity thresholds determined at rest, stressing the critical link between spatial resolution and pattern recognition. In a subsequent study, Tremblay and colleagues (Master, Larue et al. 2010) compared tactile letter recognition across three age groups, youth, young adults and seniors. The performance was monitored not only in terms of accuracy but also in terms of response time. The comparison revealed a major age effect on performance with youth and young adults largely outperforming the seniors performance both in terms of accuracy (20% decline) and response time. The latter outcome was particularly affected by age, seniors showing a 2-3 × increase in response time. Thus, pattern recognition appears to become much less efficient with age, with decreasing accuracy and longer processing time.

Texture perception

Perception of texture by touch has two main dimensions: the roughness-smoothness continuum and the hardness-softness continuum. Only the former has been the subject of systematic investigations. Psychophysical studies conducted by Lederman et al. in the 70s (Lederman and Taylor 1972, Lederman 1974, Lederman 1978) using mechanical gratings have contributed significantly in our understanding of texture perception. These studies revealed that spacing between repeated elements (e.g. groove width in a grating) was a major determinant of perceived roughness (Lederman 1982). This work and subsequent investigations have also shown that the ability to perceive relative roughness was quite refined, observers being able to reliably detect increase in spatial period of 1-3% between gratings (Lamb 1983). Only a handful of studies have actually examined changes in texture perception with age. Sathian, Zangaladze et al. (1997) reported on the relatively good performance exhibited by healthy seniors in discriminating grating roughness when compared to that of age-matched senior patients affected by Parkinson’s disease (difference threshold, 4% vs. 14%, respectively). Along the same line, Tremblay, Mireault et al. (2002), in investigating the impact of computer usage on tactile perception, showed that roughness discrimination of gratings was largely unaffected by the degree of exposure or by age. More recently, Bowden and McNulty (2013) compared texture discrimination in different age groups and concluded that performance of seniors was largely comparable to that of younger participants. Thus, it seems that, unlike other forms of tactile abilities, the perception of surface texture remains relatively impervious to the effect of age.

Tactile recognition of 3-D objects

Tactile gnosis or stereognosis refers to the ability to recognize common objects by touch. Such recognition involves a complex process whereby material (e.g., texture, compliance) and geometrical properties (e.g., shape) are first extracted by manual exploration and then integrated centrally to allow for proper identification. Performance is usually assessed by asking participants to recognize a series of familiar objects placed in their hand and by recording the response time and overall accuracy (Jones 1989). In general, healthy people can recognize familiar objects placed in their hand within 3 sec (Jones 1989). Another form of test to assess tactile gnosis is to ask participants to explore an object and then match it with a sample of objects having similar shapes. Although we rely on it almost every day, tactile recognition of 3-D objects has not been extensively studied, especially with regard to the effect of aging. Ballesteros and colleagues (Ballesteros and Reales 2004, Ballesteros, Reales et al. 2008) investigated the influence of priming in the ability of participants (healthy young, senior adults and patients with dementia) to recognize common 3-D objects (e.g. tools) via haptic touch. Participants were first allowed to tactually explore a sample of different objects for 10 s. Then, in a second testing session, some of the previously explored objects were presented along with new “unexplored” objects. Their results showed a clear priming effect for faster recognition of previously “explored” objects when compared to “unexplored” objects. Interestingly, this priming effect was present in both young and older participants and of similar magnitude, indicating that healthy seniors were as susceptible as younger participants to haptic priming. In the same vein, Norman, Crabtree et al. (2006) compared the ability of younger and older participants to discriminate 3-D objects with familiar shape (Bell peppers) and found no difference in performance between the two groups. In a subsequent study (Norman, Kappers et al. 2011), the same investigators examined whether age affects the ability to perceive large and small 3D objects by haptic touch. The large objects were explored using the whole hand whereas the small objects were explored with a single finger. In both tasks, the performance in recognizing shapes of the older group was as accurate and precise as that of the younger group. From this limited set of observations, it appears that the ability to recognize 3-D objects by haptic exploration is largely preserved with advancing age.

Why are some tactile abilities more affected than others by advancing age?

As we saw in the preceding sections, some forms of touch perception seem to be particularly affected by advancing age (e.g. pressure sensitivity) while others seem largely preserved (e.g. texture discrimination). Such observations reflect differences in the effects of advancing age on the various neurophysiological mechanisms underlying tactile perception.

For instance, at the peripheral level, age-dependent reductions in the density of receptors supplying the glabrous skin (Cauna 1965, Bruce 1980) might account for the substantial decline observed in the ability to resolve spatial details, irrespective of the mode of touch (tactile or haptic sensing). Similarly, decreased sensitivity to mechanical pressure or vibration may also reflect age-related change in both the number and in the transduction properties of peripheral receptors such as Merkel’ discs, Meissner’s and Pacini corpuscles (Kenshalo 1986, Gescheider, Edwards et al. 1996). Interestingly, changes in the skin itself seem to have only a negligible contribution to age-related loss in tactile sensibility (Woodward 1992, Vega-Bermudez and Johnson 2004).

In addition to receptors in the periphery, there are also changes with age occurring centrally affecting the processing of tactile information. For example, early EEG studies in the 1970s and 80s described changes in somatosensory evoked potentials with age including longer latencies and smaller amplitudes (Lüders 1970, Allison, Hume et al. 1984). More recent work using advanced imaging techniques has corroborated these early neurophysiological findings (e.g., Sebastian, Reales et al. 2011) and suggests that such changes are indicative of aging effects inducing both slower tactile sensory processing possibly due to age-related demyelination of axons as well as somatosensory cortical atrophy resulting in fewer neurons available for sensory processing at the cortical level (Raz, Gunning et al. 1997, Gunning-Dixon, Head et al. 1998, Abe, Aoki et al. 2002, Good, Johnsrude et al. 2002, Raz, Rodrigue et al. 2003, Raz, Gunning-Dixon et al. 2004, Salat, Buckner et al. 2004, Hsu, Leemans et al. 2008). Indirect evidence for impaired central processing with age was obtained by Master, Larue et al. (2010) when examining the performance of a group of healthy seniors in recognizing raised letters by touch. While seniors exhibited relatively good accuracy, their response times were substantially longer than those observed in young adults, indicating slower processing possibly linked with impaired tactile working memory.

Thus both changes at the peripheral and central level might contribute to impaired performance with age in the ability to detect near-threshold stimuli, or to process fine spatial details. Conversely, when tasks are based on above threshold stimulation and do not involve fine spatial discrimination, then seniors can show performance levels comparable to those seen in the younger population. This is likely the case for roughness perception, where discrimination performance relies largely on intensity signaling at the cortical level (Sinclair and Burton 1991, Jiang, Tremblay et al. 1997). The same applies for the recognition of common 3-D objects, where the multiple sources of information available (e.g., shape, temperature, consistence) might ease the identification even if one source is not reliable.

On a final note, one may ask whether expertise in manual tasks could potentially counteract age-related changes in tactile performance. Two recent studies have examined this question. In one study, Reuter, Voelcker-Rehage et al. (2012) examined whether work-related expertise in manual tasks influenced performance in a variety of tasks assessing tactile and haptic sensing abilities. Their results showed that only the older workers (54-65 years) exhibited signs of declining performance when compared to young and middle-aged workers. In addition, their results showed no influence of tactile expertise on age-related changes in performance. In investigating the same question, Guest, Mehrabyan et al. (2014) reached a similar conclusion. Their results showed that degrees of tactile expertise had no relationship with performance levels measured in different tests evaluating tactile and haptic sensing abilities. While manual expertise and tactile experience might not drastically change the course of age-related decline in most seniors, the story might be different for those seniors who had to adjust to a loss in functional vision at some point in their life. In fact, a study by Legge and colleagues (2008) showed that blind braille readers, unlike sighted subjects, did not experience decline with age on a 2D haptic test, which suggests that extensive tactile experience (or some other feature related blindness) may be able to overcome the impact of age on tactile performance.

Conclusion

As we have seen through this chapter, much like the other senses, the sense of touch tends to decline as we age. This decline, however, is not uniform across individuals, some being more affected than others. The decline is also more noticeable in certain forms of touch perception (e.g. spatial discrimination), leaving other forms relatively preserved (e.g., 3-D object recognition). Interestingly, factors such as mechanical changes in the skin seem to play a minor role in mediating age-related changes; pointing to the importance of alterations in the somatosensory system both at the level of peripheral receptors and centrally. Further evidence for the importance of central factors in influencing age-related changes in tactile performance, comes from observations on blind people showing that extensive practice over a lifetime can somehow help to counteract the decline in sensitivity associated with advancing age.

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