A Genetic Basis for Mechanosensory Traits in Humans

Frenzel, H; Bohlender, Jürgen; Pinsker, Katrin; Wohlleben, Bärbel; Tank, Jens; Lechner, Stefan; Schiska, Daniela; Jaijo, Teresa; Rüschendorf, Franz; Saar, Kathrin; Jordan, Jens; Millán, José María; Gross, Manfred; Lewin, Gary R.

doi:10.1371/journal.pbio.1001318

Cited by 66 publications

(71 citation statements)

References 71 publications

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“…Mice were able to report a temperature reduction of 2 ˚C from skin temperature with high success rates (Fig. 1d), placing mouse cooling detection performance in a similar range as that of healthy humans 1,2 .…”

Section: A Temperature Perception Task For Head-restrained Micementioning

confidence: 77%

A somatosensory circuit for cooling perception in mice

et al. 2014

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The temperature of an object provides important somatosensory information for animals performing tactile tasks. Humans can perceive skin cooling of less than one degree, but the sensory afferents and central circuits they engage to enable the perception of surface temperature are poorly understood. To address these questions, we examined the perception of glabrous skin cooling in mice. We found that mice were also capable of perceiving small amplitude skin cooling and that primary somatosensory (S1) cortical neurons were required for cooling perception. Moreover, the absence of the menthol-gated transient receptor potential melastatin 8 ion channel in sensory afferent fibers eliminated the ability to perceive cold and the corresponding activation of S1 neurons. Our results identify parts of a neural circuit underlying cold perception in mice and provide a new model system for the analysis of thermal processing and perception and multimodal integration.An accurate sense of surface temperature helps animals to perceive object structure and identity. Psychophysical experiments have shown that humans are able to perceive tiny changes in skin cooling with a range between 0.4 and 1.8 ˚C 1,2 . It has, however, proved challenging to assess the perceptual ability of rodents to discriminate small temperature steps at threshold levels.Classical paw withdrawal tests cannot differentiate between reflexive avoidance behavior and sensory perception 3 . Two-plate thermal preference arenas have shown that mice avoid cooler floor temperatures [4][5][6] , but this test has limited spatial and temporal control of the stimulus and lacks fine-grained resolution for near threshold perception. We therefore developed a shortlatency, goal-directed thermal perception task using the glabrous skin of the mouse forepaw.A general dogma is that all somatosensory input, including thermal, is integrated by the primary somatosensory cortex (S1) to form a coherent sensory percept. S1 is necessary for tactile somatosensory perception in rodents [7][8][9][10][11][12][13] . The role of S1 in thermal perception, however, is under debate, 3 with three studies concluding that rodent S1 is not involved [14][15][16] and another concluding that it is 17 . This may be because these studies used large cortical lesions with long recovery and retraining periods in freely moving rats that used facial regions to detect temperature [14][15][16][17] .Likewise, very little is known about the underlying cortical neural processing of non-noxious thermal stimuli in rodents. To the best of our knowledge, only one study, conducted in anesthetized rats stimulating scrotal skin, has shown extracellular responses of cortical neurons to thermal stimulation 18 . At the sensory periphery, a range of primary afferents including myelinated Aβ mechanoreceptors 2,19 , thinly myelinated Aδ-fibers and unmyelinated polymodal C fibers, fire during skin cooling 4,20,21 . Although it is thought that thickly myelinated Aδ fibers are responsible for cooling perception, C fibers ...

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Section: A Temperature Perception Task For Head-restrained Micementioning

confidence: 77%

A somatosensory circuit for cooling perception in mice

et al. 2014

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“…Indeed, a recent twin study provides evidence that touch sensitivity is heritable and correlated with hearing acuity (Frenzel et al 2012). Further support for this sensory evolution hypothesis comes from a recent study that provides convincing evidence that the middle ear bones evolved from bones in the jaw (Meng et al 2011) and that cells in the inner ear and those found in the lateral lines of fish share a common genetic origin.…”

Section: Implications For Multisensory Interactionsmentioning

confidence: 95%

A neural link between feeling and hearing

Ellmore

Beauchamp

2012

Seeing and Perceiving

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Hearing and feeling both rely upon the transduction of physical events into frequency-based neural codes, suggesting that the auditory system may be intimately related to the somatosensory system. Here, we provide evidence that the neural substrates for audition and somatosensation are anatomically linked. Using diffusion tensor imaging with both deterministic and probabilistic tractography to measure white matter connectivity, we show that there are extensive ipsilateral connections between the primary auditory cortex and the primary and secondary somatosensory regions in the human cerebral cortex. We further show that these crossmodal connections are exaggerated between the auditory and secondary somatosensory cortex in the lesioned hemisphere of a patient (SR) with acquired auditory-tactile synesthesia, in whom sounds alone produce bodily sensations. These results provide an anatomical basis for multisensory interactions between audition and somatosensation and suggest that cross-talk between these regions may explain why some sounds, such as nails screeching down a chalkboard or an audible mosquito, can induce feelings of touch, especially on the contralesional body surface of patient SR.

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“…In perception, there are strong relationships between touch and audition, likely because both senses share common genetic factors related to mechanoreception (Frenzel et al, 2012). In visual perception, there is a long history of relating visual performance or susceptibility to illusions to personality, intelligence, or cognition and other visual functions (Coren & Porac, 1987;Galton, 1883;Gregory, 2004;Jensen, 2002;Piaget, 1969;Roff, 1953;Spearman, 1904;Thurstone, 1938Thurstone, , 1944.…”

Section: Introductionmentioning

confidence: 99%

About individual differences in vision

et al. 2017

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a b s t r a c tIn cognition, audition, and somatosensation, performance strongly correlates between different paradigms, which suggests the existence of common factors. In contrast, visual performance in seemingly very similar tasks, such as visual and bisection acuity, are hardly related, i.e., pairwise correlations between performance levels are low even though test-retest reliability is high. Here we show similar results for visual illusions. Consistent with previous findings, we found significant correlations between the illusion magnitude of the Ebbinghaus and Ponzo illusions, but this relationship was the only significant correlation out of 15 further comparisons. Similarly, we found a significant link for the Ponzo illusion with both mental imagery and cognitive disorganization. However, most other correlations between illusions and personality were not significant. The findings suggest that vision is highly specific, i.e., there is no common factor. While this proposal does not exclude strong and stable associations between certain illusions and between certain illusions and personality traits, these associations seem to be the exception rather than the rule.

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A Genetic Basis for Mechanosensory Traits in Humans

Abstract: Hearing and touch are genetically related, and people with excellent hearing are more likely to have a fine sense of touch and vice versa.

Cited by 66 publications

References 71 publications

A somatosensory circuit for cooling perception in mice

A somatosensory circuit for cooling perception in mice

A neural link between feeling and hearing

About individual differences in vision

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