Review
Thermal sensitivity in the elderly: A review

https://doi.org/10.1016/j.arr.2010.04.009Get rights and content

Abstract

Aging is associated with a progressive decrease in thermal perception, as revealed by increased thermal detection thresholds in the elderly. This reduction in thermosensitivity follows a distal–proximal pattern, with more pronounced decrements observed in the limbs and in the perception of warmth vs. cold. The main underlying causes of this seem to be aging of the skin and subsequent reductions in thermoreceptor density and superficial skin blood flow. However, the results from some animal studies also suggest that changes in the peripheral nerve system, particularly fiber loss and decreased conduction velocity, may also be involved. In this paper, we review age-related changes in the thermal sensitivity of humans, their underlying mechanisms, and the strengths and limitations of some of the methodologies used to assess these changes.

Introduction

From a neuroanatomical standpoint, thermal sensitivity relies on components of the peripheral and the central nervous systems such as: the cutaneous free nerve endings and the Aδ and C primary afferent fibers; the secondary somatosensory neurons in the dorsal horn of the spinal cord; the spinothalamic tractus; the thalamus; and the primary and secondary somatosensory cortices. Age significantly influences the structures and functions of the nervous system, leading to age-related changes in thermal perception. Moreover, structural changes in aging skin affect the functionality of the skin's temperature receptors, thereby altering thermal perception.

Within the field of psychophysics, a number of tools have been developed for quantitatively assessing sensations; these include the threshold and suprathreshold measures, tolerance, perceived intensity, and perceived quality of stimuli. While a large body of literature generally agrees regarding the effects of aging on visual and auditory senses, relatively less work has been devoted to examining thermal perception in the elderly. Age-related declines in thermal sensitivity have been reported, but the evidence of decreased sensitivity varies depending on the methodology, the body region(s) under consideration, the type of measures used (threshold vs. suprathreshold), and the modality of the utilized stimuli (warm vs. cold). Furthermore, although several factors have been hypothesized to account for age-related decreases in thermal senses, the actual underlying mechanisms are still obscure.

The present paper reviews studies on age-related changes in human thermal sensitivity. After a brief presentation of the neurophysiological and neuroanatomical bases of the thermal senses in humans, quantitative sensory explorations from the past few decades are presented and discussed. Finally, some potential underlying mechanisms are examined and further research directions are suggested.

Section snippets

The neurophysiological bases of thermal sensitivity in humans

Thermal sensations arise in response to relatively small temperature changes at the body surface; depending on their direction, these changes are perceived as warming or cooling (Hensel, 1973). The specificity theory of somesthesis (Boring, 1942) holds that perceptions of cold and warm are served by separate senses. Indeed, these perceptions appear to rely on separate neural pathways involving thin myelinated or unmyelinated axons of the peripheral nervous system (Hensel, 1974, Hensel et al.,

Studying thermal sensitivity in human elderly

The most common methodology that has been used to investigate thermal sensitivity is similar to that used for other sensory systems, and involves the measurement of perception thresholds. The computer revolution enabled the translation of various test algorithms to automated sequences and result calculation. Another technical advent was the Peltier principle (i.e., the direct conversion of electric voltage to temperature differences) which permitted the development of contact thermal

Innocuous thermal stimuli

In a seminal paper on the effects of age on somesthetic sensitivity (see Table 1 for a description of studies on innocuous thermal thresholds), Kenshalo (1986) assessed the absolute detection thresholds of cold, warm, heat pain, and vibration at two body sites (thenar eminence and foot sole) in 27 young individuals (aged 19–31) and 21 elderly people (aged 55–84). This study was one of the first to establish that age could selectively influence one sensory modality (vibrotactile) but not another

Underlying mechanisms

Thermal perception decreases with age, as shown by studies on thermal thresholds, CHEPs, and LEPs. Several factors may account for such age-dependent losses in human thermal perception, including aging processes in the skin and peripheral nerve system. Increases in thermal thresholds and changes in CHEPs and LEPs may thus be subsequent to a decrease in skin innervation, reduced skin blood flow, and/or neuron loss in or dysfunction of peripheral nerves. This Section presents data from human and

Conclusions

Thermal perception in humans seems to decrease progressively with age, following a distal–proximal pattern of decline and showing a greater loss of sensation in the lower limbs. Both warm and cold sensitivities are decreased in the elderly, but the degree of retained cold sensitivity generally predominates over the remaining warm sensitivity. Several related mechanisms have been proposed to explain the observed reduction in sensitivity, including age effects on the coetaneous and peripheral

References (154)

  • N.A. Fenske et al.

    Structural and functional changes of normal aging skin

    J. Am. Acad. Dermatol.

    (1986)
  • G.B. Freeman et al.

    Selective alteration of mouse brain neurotransmitter release with age

    Neurobiol. Aging

    (1987)
  • H. Fruhstorfer et al.

    The significance of A-delta and C fibres for the perception of synthetic heat

    Eur. J. Pain

    (2003)
  • D.A. Gelber et al.

    Components of variance for vibratory and thermal threshold testing in normal and diabetic subjects

    J. Diabetes Complications

    (1995)
  • F. Gerr et al.

    Covariates of human peripheral nerve function. II. Vibrotactile and thermal thresholds

    Neurotoxicol. Teratol.

    (1994)
  • S.J. Gibson et al.

    Altered heat pain thresholds and cerebral event-related potentials following painful CO2 laser stimulation in subjects with fibromyalgia syndrome

    Pain

    (1994)
  • Y. Granovsky et al.

    Thermoreceptive innervation of human glabrous and hairy skin: a contact heat evoked potential analysis

    Pain

    (2005)
  • Y. Granovsky et al.

    Objective correlate of subjective pain perception by contact heat-evoked potentials

    J. Pain

    (2008)
  • W. Greffrath et al.

    Peripheral and central components of habituation of heat pain perception and evoked potentials in humans

    Pain

    (2007)
  • M.J. Hilz et al.

    Early diagnosis of diabetic small fiber neuropathy by disturbed cold perception

    J. Diabetes Complications

    (1988)
  • D.R. Kenshalo et al.

    Some response properties of cold fibers to cooling

    Prog. Brain Res.

    (1976)
  • M.L. Ko et al.

    The effects of aging on spinal neurochemistry in the rat

    Brain Res. Bull.

    (1997)
  • G. Lauria et al.

    Epidermal innervation: changes with aging, topographic location, and in sensory neuropathy

    J. Neurol. Sci.

    (1999)
  • J.C. Arezzo et al.

    Thermal sensitivity tester. Device for quantitative assessment of thermal sense in diabetic neuropathy

    Diabetes

    (1986)
  • D.D. Atherton et al.

    Use of the novel Contact Heat Evoked Potential Stimulator (CHEPS) for the assessment of small fibre neuropathy: correlations with skin flare responses and intra-epidermal nerve fibre counts

    BMC Neurol.

    (2007)
  • A.K. Balin et al.

    Physiological consequences of human skin aging

    Cutis

    (1989)
  • G. Bartlett et al.

    Normal distributions of thermal and vibration sensory thresholds

    Muscle Nerve

    (1998)
  • N. Becser et al.

    Reliability of cephalic thermal thresholds in healthy subjects

    Cephalalgia

    (1998)
  • H.H. Berman et al.

    Representation of nociceptive stimuli in primary sensory cortex

    Neuroreport

    (1998)
  • F.W. Bertelsmann et al.

    Thermal discrimination thresholds in normal subjects and in patients with diabetic neuropathy

    J. Neurol. Neurosurg. Psychiatry

    (1985)
  • I. Besne et al.

    Effect of age and anatomical site on density of sensory innervation in human epidermis

    Arch. Dermatol.

    (2002)
  • P. Bessou et al.

    Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli

    J. Neurophysiol.

    (1969)
  • M. Blix

    Experimentelle Beiträge zur Lösung der Frage über die spezifische Energie der Hautnerven

    Zeitschrift für Biologie

    (1884)
  • E.G. Boring

    Tactual Sensibility, Sensation and Perception in the History of Experimental Psychology

    (1942)
  • P. Bouche et al.

    Clinical and electrophysiological study of the peripheral nervous system in the elderly

    J. Neurol.

    (1993)
  • B. Bravenboer et al.

    Thermal threshold testing for the assessment of small fibre dysfunction: normal values and reproducibility

    Diabet. Med.

    (1992)
  • B. Bromm et al.

    Laser-evoked cerebral potentials in the assessment of cutaneous pain sensitivity in normal subjects and patients

    Rev. Neurol. (Paris)

    (1991)
  • M. Campero et al.

    C-polymodal nociceptors activated by noxious low temperature in human skin

    J. Physiol.

    (1996)
  • M. Campero et al.

    Slowly conducting afferents activated by innocuous low temperature in human skin

    J. Physiol. (Lond.)

    (2001)
  • D. Ceballos et al.

    Morphometric and ultrastructural changes with ageing in mouse peripheral nerve

    J. Anat.

    (1999)
  • D. Cerimele et al.

    Physiological changes in ageing skin

    Br. J. Dermatol.

    (1990)
  • Y.C. Chang et al.

    Effects of aging on human skin innervation

    Neuroreport

    (2004)
  • C.C. Chao et al.

    Effects of aging on contact heat-evoked potentials: the physiological assessment of thermal perception

    Muscle Nerve

    (2007)
  • A.B. Chatt et al.

    Cerebral evoked responses to skin warming recorded from human scalp

    Exp. Brain Res.

    (1977)
  • I.A. Chen et al.

    Contact heat evoked potentials in normal subjects

    Acta Neurol. Taiwan

    (2006)
  • D. Claus et al.

    Methods of measurement of thermal thresholds

    Acta Neurol. Scand.

    (1987)
  • D. Claus et al.

    Thermal discrimination thresholds: a comparison of different methods

    Acta Neurol. Scand.

    (1990)
  • K.J. Collins et al.

    Urban hypothermia: preferred temperature and thermal perception in old age

    Br. Med. J. (Clin. Res. Ed.)

    (1981)
  • G. Cruccu et al.

    Assessment of trigeminal small-fiber function: brain and reflex responses evoked by CO2-laser stimulation

    Muscle Nerve

    (1999)
  • J.N. de Neeling et al.

    Sensory thresholds in older adults: reproducibility and reference values

    Muscle Nerve

    (1994)
  • Cited by (155)

    View all citing articles on Scopus
    View full text