Emotions alter muscle proprioceptive coding of movements in humans

Emotions can evoke strong reactions that have profound influences, from gross changes in our internal environment to small fluctuations in facial muscles, and reveal our feelings overtly. Muscles contain proprioceptive afferents, informing us about our movements and regulating motor activities. Their firing reflects changes in muscle length, yet their sensitivity can be modified by the fusimotor system, as found in animals. In humans, the sensitivity of muscle afferents is modulated by cognitive processes, such as attention; however, it is unknown if emotional processes can modulate muscle feedback. Presently, we explored whether muscle afferent sensitivity adapts to the emotional situation. We recorded from single muscle afferents in the leg, using microneurography, and moved the ankle joint of participants, while they listened to evocative classical music to induce sad, neutral, or happy emotions, or sat passively (no music). We further monitored their physiological responses using skin conductance, heart rate, and electromyography measures. We found that muscle afferent firing was modified by the emotional context, especially for sad emotions, where the muscle spindle dynamic response increased. We suggest that this allows us to prime movements, where the emotional state prepares the body for consequent behaviour-appropriate reactions.

[1]  U. Windhorst Muscle proprioceptive feedback and spinal networks , 2007, Brain Research Bulletin.

[2]  Kelly M. Naugle,et al.  Emotional state affects gait initiation in individuals with Parkinson’s disease , 2012, Cognitive, affective & behavioral neuroscience.

[3]  N. Kakuda Response of human muscle spindle afferents to sinusoidal stretching with a wide range of amplitudes , 2000, The Journal of physiology.

[4]  Frank Huethe,et al.  Suppression of Enhanced Physiological Tremor via Stochastic Noise: Initial Observations , 2014, PloS one.

[5]  M Esslen,et al.  Brain areas and time course of emotional processing , 2004, NeuroImage.

[6]  Isabelle Peretz,et al.  Role of tempo entrainment in psychophysiological differentiation of happy and sad music? , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  S. Gandevia,et al.  The kinaesthetic senses , 2009, The Journal of physiology.

[8]  Carlos M. Coelho,et al.  Increased corticospinal excitability induced by unpleasant visual stimuli , 2010, Neuroscience Letters.

[9]  Assal Habibi,et al.  The pleasures of sad music: a systematic review , 2015, Front. Hum. Neurosci..

[10]  Valérie Hospod,et al.  Fusimotor drive may adjust muscle spindle feedback to task requirements in humans. , 2009, Journal of neurophysiology.

[11]  Michael Dimitriou,et al.  Enhanced Muscle Afferent Signals during Motor Learning in Humans , 2016, Current Biology.

[12]  M. Tervaniemi,et al.  It's Sad but I Like It: The Neural Dissociation Between Musical Emotions and Liking in Experts and Laypersons , 2016, Front. Hum. Neurosci..

[13]  Thierry Gélat,et al.  Gait initiation is affected during emotional conflict , 2011, Neuroscience Letters.

[14]  H. Johansson,et al.  Fusimotor reflexes in triceps surae elicited by natural stimulation of muscle afferents from the cat ipsilateral hind limb , 1982, The Journal of physiology.

[15]  Charles H Hillman,et al.  Emotion and motivated behavior: postural adjustments to affective picture viewing , 2004, Biological Psychology.

[16]  S. Khalfa,et al.  Event-related skin conductance responses to musical emotions in humans , 2002, Neuroscience Letters.

[17]  P. Matthews,et al.  After‐effects of fusimotor stimulation on the response of muscle spindle primary afferent endings , 1969, The Journal of physiology.

[18]  M. Hulliger,et al.  The mammalian muscle spindle and its central control. , 1984, Reviews of physiology, biochemistry and pharmacology.

[19]  C. Krumhansl An exploratory study of musical emotions and psychophysiology. , 1997, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[20]  Jennifer C. Britton,et al.  Facial expressions and complex IAPS pictures: Common and differential networks , 2006, NeuroImage.

[21]  Phillip Wolff,et al.  Causal reasoning with forces , 2015, Front. Hum. Neurosci..

[22]  A. Prochazka,et al.  Ia afferent activity during a variety of voluntary movements in the cat , 1977, The Journal of physiology.

[23]  R. Zatorre,et al.  The Rewarding Aspects of Music Listening Are Related to Degree of Emotional Arousal , 2009, PloS one.

[24]  D. Burke,et al.  Effect of training on voluntary activation of human fusimotor neurons. , 1985, Journal of neurophysiology.

[25]  C. Ghez,et al.  Loss of proprioception produces deficits in interjoint coordination. , 1993, Journal of neurophysiology.

[26]  N Kakuda,et al.  Dynamic response of human muscle spindle afferents to stretch during voluntary contraction , 1998, Journal of Physiology.

[27]  P. Matthews The differentiation of two types of fusimotor fibre by their effects on the dynamic response of muscle spindle primary endings. , 1962, Quarterly journal of experimental physiology and cognate medical sciences.

[28]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  Jejo D. Koola,et al.  Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. , 2007, Psychophysiology.

[30]  T. Pozzo,et al.  Motor planning of goal-directed action is tuned by the emotional valence of the stimulus: a kinematic study , 2016, Scientific reports.

[31]  D. Burke,et al.  Does the nervous system depend on kinesthetic information to control natural limb movements , 1992 .

[32]  J C Rothwell,et al.  Manual motor performance in a deafferented man. , 1982, Brain : a journal of neurology.

[33]  M Hulliger,et al.  Effects of combining static and dynamic fusimotor stimulation on the response of the muscle spindle primary ending to sinusoidal stretching. , 1977, The Journal of physiology.

[34]  R. K. Beals THE JOINTS OF THE ANKLE , 1977 .

[35]  Emmanuel Bigand,et al.  The Time Course of Emotional Responses to Music , 2005, Annals of the New York Academy of Sciences.

[36]  V. Della-Maggiore,et al.  Corticospinal Excitability Preceding the Grasping of Emotion-Laden Stimuli , 2014, PloS one.

[37]  Brown Mc,et al.  After‐effects of fusimotor stimulation on the response of muscle spindle primary afferent endings , 1969, The Journal of physiology.

[38]  C. Janelle,et al.  Emotion and movement: Activation of defensive circuitry alters the magnitude of a sustained muscle contraction , 2006, Neuroscience Letters.

[39]  P. Johnson-Laird,et al.  The language of emotions: An analysis of a semantic field , 2013 .

[40]  E. Ribot-Ciscar,et al.  Changes in Human Muscle Spindle Sensitivity during a Proprioceptive Attention Task , 2007, The Journal of Neuroscience.

[41]  I. Peretz,et al.  Music and emotion: perceptual determinants, immediacy, and isolation after brain damage , 1998, Cognition.

[42]  B. Wallin,et al.  Resting discharge of human muscle spindles is not modulated by increases in sympathetic drive , 2003, The Journal of physiology.

[43]  P. Zangger,et al.  ‘Fusimotor set’: new evidence for α-independent control of γ-motoneurones during movement in the awake cat , 1985, Brain Research.

[44]  Steven C. R. Williams,et al.  A functional MRI study of happy and sad affective states induced by classical music , 2007, Human brain mapping.

[45]  J. Cacioppo,et al.  Electromyographic activity over facial muscle regions can differentiate the valence and intensity of affective reactions. , 1986, Journal of personality and social psychology.

[46]  Simon C. Gandevia,et al.  Kinesthesia and unique solutions for control of multijoint movements , 1992, Behavioral and Brain Sciences.

[47]  David C. Alsop,et al.  Brain Activation during Facial Emotion Processing , 2002, NeuroImage.

[48]  B. Edin,et al.  Classification of human muscle stretch receptor afferents: a Bayesian approach. , 1990, Journal of neurophysiology.

[49]  K. R. Ridderinkhof,et al.  Emotional stimuli modulate readiness for action: A transcranial magnetic stimulation study , 2010, Cognitive, affective & behavioral neuroscience.

[50]  J. Wessberg,et al.  Fusimotor and skeletomotor activities are increased with precision finger movement in man. , 1996, The Journal of physiology.

[51]  Vittorio Gallese,et al.  Modulation of Arm Reaching Movements during Processing of Arm/Hand-Related Action Verbs with and without Emotional Connotation , 2014, PloS one.

[52]  Isabelle Peretz,et al.  The “Musical Emotional Bursts”: a validated set of musical affect bursts to investigate auditory affective processing , 2013, Front. Psychol..

[53]  A. Vallbo,et al.  Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. , 1968, Experimental neurology.

[54]  Liliane Borel,et al.  Improving postural control by applying mechanical noise to ankle muscle tendons , 2016, Experimental Brain Research.

[55]  V. Gazzola,et al.  Temporal dynamics of motor cortex excitability during perception of natural emotional scenes. , 2014, Social cognitive and affective neuroscience.

[56]  A B Vallbo,et al.  Human muscle spindle response in a motor learning task. , 1990, The Journal of physiology.

[57]  D. Burke,et al.  Discharge of human muscle spindle afferents innervating ankle dorsiflexors during target isometric contractions , 1997, The Journal of physiology.

[58]  Vaughan G. Macefield,et al.  Contributions of Central Command and Muscle Feedback to Sympathetic Nerve Activity in Contracting Human Skeletal Muscle , 2016, Front. Physiol..

[59]  B. Edin,et al.  Human Muscle Spindles Act as Forward Sensory Models , 2010, Current Biology.

[60]  Lutz Jäncke,et al.  Modulation of corticospinal activity by strong emotions evoked by pictures and classical music: a transcranial magnetic stimulation study , 2007, Neuroreport.

[61]  C. Tallon-Baudry,et al.  The neural subjective frame: from bodily signals to perceptual consciousness , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[62]  J. Sanes,et al.  Motor control in humans with large-fiber sensory neuropathy. , 1985, Human neurobiology.

[63]  T. Baumgartner,et al.  From emotion perception to emotion experience: emotions evoked by pictures and classical music. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[64]  J. Summers,et al.  Emotion and motor preparation: A transcranial magnetic stimulation study of corticospinal motor tract excitability , 2009, Cognitive, affective & behavioral neuroscience.

[65]  P. Matthews Where does Sherrington's "muscular sense" originate? Muscles, joints, corollary discharges? , 1982, Annual review of neuroscience.

[66]  Lutz Jäncke,et al.  The emotional power of music: How music enhances the feeling of affective pictures , 2006, Brain Research.

[67]  A Prochazka,et al.  'Fusimotor set': new evidence for alpha-independent control of gamma-motoneurones during movement in the awake cat. , 1985, Brain research.