Neuroscience of rhythm

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The neuroscience of rhythm refers to the various forms of rhythm generated by the central nervous system (CNS). Nerve cells, also known as neurons in the human brain are capable of firing in specific patterns which cause oscillations. The brain possesses many different types of oscillators with different periods. Oscillators are simultaneously outputting frequencies from .02 Hz to 600 Hz. It is now well known that a computer is capable of running thousands of processes with just one high-frequency clock. Humans have many different clocks as a result of evolution. Prior organisms had no need for a fast-responding oscillator. This multi-clock system permits quick response to constantly changing sensory input while still maintaining the autonomic processes that sustain life. This method modulates and controls a great deal of bodily functions. [1]

Contents

Autonomic rhythms

The autonomic nervous system is responsible for many of the regulatory processes that sustain human life. Autonomic regulation is involuntary, meaning we do not have to think about it for it to take place. A great deal of these are dependent upon a certain rhythm, such as sleep, heart rate, and breathing.

Circadian rhythms

Circadian literally translates to "about a day" in Latin. This refers to the human 24-hour cycle of sleep and wakefulness. This cycle is driven by light. The human body must photoentrain or synchronize itself with light in order to make this happen. The rod cells are the photoreceptor cells in the retina capable of sensing light. However, they are not what sets the biological clock. The photosensitive retinal ganglion cells contain a pigment called melanopsin. This photopigment is depolarized in the presence of light, unlike the rods which are hyperpolarized. Melanopsin encodes the day-night cycle to the suprachiasmatic nucleus (SCN) via the retinohypothalamic tract. The SCN evokes a response from the spinal cord. Preganglionic neurons in the spinal cord modulate the superior cervical ganglia, which synapses on the pineal gland. The pineal gland synthesizes the neurohormone melatonin from tryptophan. Melatonin is secreted into the bloodstream where it affects neural activity by interacting with melatonin receptors on the SCN. The SCN is then able to influence the sleep wake cycle, acting as the "apex of a hierarchy" that governs physiological timing functions. [2] "Rest and sleep are the best example of self-organized operations within neuronal circuits". [1]

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Sleep and memory have been closely correlated for over a century. It seemed logical that the rehearsal of learned information during the day, such as in dreams, could be responsible for this consolidation. REM sleep was first studied in 1953. It was thought to be the sole contributor to memory due to its association with dreams. It has recently been suggested that if sleep and waking experience are found to be using the same neuronal content, it is reasonable to say that all sleep has a role in memory consolidation. This is supported by the rhythmic behavior of the brain. Harmonic oscillators have the capability to reproduce a perturbation that happened in previous cycles. It follows that when the brain is unperturbed, such as during sleep, it is in essence rehearsing the perturbations of the day. Recent studies have confirmed that off-wave states, such as slow-wave sleep, play a part in consolidation as well as REM sleep. There have even been studies done implying that sleep can lead to insight or creativity. Jan Born, from the University of Lubeck, showed subjects a number series with a hidden rule. She allowed one group to sleep for three hours, while the other group stayed awake. The awake group showed no progress, while most of the group that was allowed to sleep was able to solve the rule. This is just one example of how rhythm could contribute to humans unique cognitive abilities. [1]

Central pattern generation

A central pattern generator (CPG) is defined as a neural network that does not require sensory input to generate a rhythm. This rhythm can be used to regulate essential physiological processes. These networks are often found in the spinal cord. It has been hypothesized that certain CPG's are hardwired from birth. For example, an infant does not have to learn how to breathe and yet it is a complicated action that involves a coordinated rhythm from the medulla. The first CPG was discovered by removing neurons from a locust. It was observed that the group of neurons was still firing as if the locust was in flight. [3] In 1994, evidence of CPG's in humans was found. A former quadrapalegic began to have some very limited movement in his lower legs. Upon lying down, he noticed that if he moved his hips just right his legs began making walking motions. The rhythmic motor patterns were enough to give the man painful muscle fatigue. [4]

A key part of CPG's is half-center oscillators. In its simplest form, this refers to two neurons capable of rhythmogenesis when firing together. The generation of a biological rhythm, or rhythmogenesis, is done by a series of inhibition and activation. For example, a first neuron inhibits a second one while it fires, however, it also induces slow depolarization in the second neuron. This is followed by the release of an action potential from the second neuron as a result of depolarization, which acts on the first in a similar fashion. This allows for self-sustaining patterns of oscillation. Furthermore, new motor patterns, such as athletic skills or the ability to play an instrument, also use half-center oscillators and are simply learned perturbations to CPG's already in place. [3]

Respiration

Ventilation requires periodic movements of the respiratory muscles. These muscles are controlled by a rhythm generating network in the brain stem. These neurons comprise the ventral respiratory group (VRG). Although this process is not fully understood, it is believed to be governed by a CPG and there have been several models proposed. The classic three phase model of respiration was proposed by D.W. Richter. It contains 2 stages of breathing, inspiratory and expiratory, that are controlled by three neural phases, inspiration, post-inspiration and expiration. Specific neural networks are dedicated to each phase. They are capable of maintaining a sustained level of oxygen in the blood by triggering the lungs to expand and contract at the correct time. This was seen by the measuring of action potentials. It was observed that certain groups of neurons synchronized with certain phases of respiration. The overall behavior was oscillatory in nature. [5] This is an example of how an autonomous biorhythm can control a crucial bodily function.

Cognition

This refers to the types of rhythm that humans are able to generate, be it from recognition of others or sheer creativity.

Sports

Muscle coordination, muscle memory, and innate game awareness all rely on the nervous system to produce a specific firing pattern in response to an either an efferent or afferent signal. Sports are governed by the same production and perception of oscillations that govern much of human activity. For example, in basketball, in order to anticipate the game one must recognize rhythmic patterns of other players and perform actions calibrated to these movements. "The rhythm of a game of basketball emerges from the rhythm of individuals, the rhythm among team members, and the rhythmic contrasts between opposing teams". [6] Although the exact oscillatory pattern that modulates different sports has not been found, there have been studies done to show a correlation between athletic performance and circadian timing. It has been shown certain times of the day are better for training and gametime performance. Training has the best results when done in the morning, while it is better to play a game at night. [7] [8]

Music

The ability to perceive and generate music is frequently studied as a way to further understand human rhythmic processing. Research projects, such as Brain Beats, [9] are currently studying this by developing beat tracking algorithms and designing experimental protocols to analyze human rhythmic processing. This is rhythm in its most obvious form. Human beings have an innate ability to listen to a rhythm and track the beat, as seen here "Dueling Banjos". [10] This can be done by bobbing the head, tapping of the feet or even clapping. Jessica Grahn and Matthew Brett call this spontaneous movement "motor prediction". They hypothesized that it is caused by the basal ganglia and the supplementary motor area (SMA). This would mean that those areas of the brain would be responsible for spontaneous rhythm generation, although further research is required to prove this. However, they did prove that the basal ganglia and SMA are highly involved in rhythm perception. In a study where patients brain activity was recorded using fMRI, increased activity was seen in these areas both in patients moving spontaneously (bobbing their head) and in those who were told to stay still. [11]

Computational models

Computational neuroscience is the theoretical study of the brain used to uncover the principles and mechanisms that guide the development, organization, information-processing and mental abilities of the nervous system. Many computational models have attempted to quantify the process of how various rhythms are created by humans. [12]

Avian song learning

Juvenile avian song learning is one of the best animal models used to study generation and recognition of rhythm. The ability for birds to process a tutor song and then generate a perfect replica of that song, underlies our ability to learn rhythm.

Two very famous computational neuroscientists Kenji Doya and Terrence J. Sejnowski created a model of this using the Zebra Finch as target organism. The Zebra Finch is perhaps one of the most easily understood examples of this among birds. The young Zebra Finch is exposed to a "tutor song" from the adult, during a critical period. This is defined as the time of life that learning can take place, in other words when the brain has the most plasticity. After this period, the bird is able to produce an adult song, which is said to be crystallized at this point. Doya and Sejnowski evaluated three possible ways that this leaning could happen, an immediate, one shot perfection of the tutor song, error learning, and reinforcement learning. They settled on the third scheme. Reinforcement learning consists of a "critic" in the brain capable of evaluating the difference between the tutor and the template song. Assuming the two are closer than the last trial, this "critic" then sends a signal activating NMDA receptors on the articulator of the song. In the case of the Zebra Finch, this articulator is the robust nucleus of archistriatum or RA. The NMDA receptors allow the RA to be more likely to produce this template of the tutor song, thus leading to learning of the correct song. [13]

Dr. Sam Sober explains the process of tutor song recognition and generation using error learning. This refers to a signal generated by the avian brain that corresponds to the error between the tutor song and the auditory feedback the bird gets. The signal is simply optimized in order to be as small of a difference as possible, which results in the learning of the song. Dr. Sober believes that this is also the mechanism employed in human speech learning. Although it's clear that humans are constantly adjusting their speech while birds are believed to have crystallized their song upon reaching adulthood. He tested this idea by using headphones to alter a Bengalese finch's auditory feedback. The bird actually corrected for up to 40% of the perturbation. This provides strong support for error learning in humans. [14]

Macaque motor cortex

This animal model has been said to be more similar to humans than birds. It has been shown that humans demonstrate 15–30 Hz (Beta) oscillations in the cortex while performing muscle coordination exercises. [15] [16] [17] This was also seen in macaque monkey cortices. The cortical local field potentials (LFPs) of conscious monkeys were recorded while they performed a precision grip task. More specifically, the pyramidal tract neurons (PTNs) were targeted for measurement. The primary frequency recorded was between 15 and 30 Hz, the same oscillation found in humans. [18] These findings indicate that the macaque monkey cortex could be a good model for rhythm perception and production. One example of how this model is used is the investigation of the role of motor cortex PTNs in "corticomuscular coherence" (muscle coordination). In similar study where LFPs were recorded from macaque monkeys while they performed a precision grip task, it was seen that the disruption of the PTN resulted in a greatly reduced oscillatory response. Stimulation of the PTN caused the monkeys to not be able to perform the grip task as well. It was concluded that PTNs in the motor cortex directly influence the generation of Beta rhythms. [19]

Imaging

Current methods

At the moment, recording methods are not capable of simultaneously measuring small and large areas at the same time, with the temporal resolution that the circuitry of the brain requires. These techniques include EEG, MEG, fMRI, optical recordings, and single-cell recordings. [1]

Future

Techniques such as large scale single-cell recordings are movements in the direction of analyzing overall brain rhythms. However, these require invasive procedures, such as tetrode implantation, which does not allow a healthy brain to be studied. Also, pharmacological manipulation, cell culture imaging and computational biology all make attempts at doing this but in the end they are indirect. [1]

Frequency bands

The classification of frequency borders allowed for a meaningful taxonomy capable of describing brain rhythms, known as neural oscillations.

ClassRange
Delta .5–4 Hz [1]
Theta 4–8 Hz [1]
Alpha 8–12 Hz [1]
Beta 12–30 Hz [1]
Gamma >30 Hz [1]

Related Research Articles

<span class="mw-page-title-main">Brain</span> Organ that controls the nervous system in vertebrates and most invertebrates

A brain is an organ that serves as the center of the nervous system in all vertebrate and most invertebrate animals. It is located in the head, usually close to the sensory organs for senses such as vision. It is the most complex organ in a vertebrate's body. In a human, the cerebral cortex contains approximately 14–16 billion neurons, and the estimated number of neurons in the cerebellum is 55–70 billion. Each neuron is connected by synapses to several thousand other neurons. These neurons typically communicate with one another by means of long fibers called axons, which carry trains of signal pulses called action potentials to distant parts of the brain or body targeting specific recipient cells.

<span class="mw-page-title-main">Nervous system</span> Part of an animal that coordinates actions and senses

In biology, the nervous system is the highly complex part of an animal that coordinates its actions and sensory information by transmitting signals to and from different parts of its body. The nervous system detects environmental changes that impact the body, then works in tandem with the endocrine system to respond to such events. Nervous tissue first arose in wormlike organisms about 550 to 600 million years ago. In vertebrates it consists of two main parts, the central nervous system (CNS) and the peripheral nervous system (PNS). The CNS consists of the brain and spinal cord. The PNS consists mainly of nerves, which are enclosed bundles of the long fibers or axons, that connect the CNS to every other part of the body. Nerves that transmit signals from the brain are called motor nerves or efferent nerves, while those nerves that transmit information from the body to the CNS are called sensory nerves or afferent. Spinal nerves are mixed nerves that serve both functions. The PNS is divided into three separate subsystems, the somatic, autonomic, and enteric nervous systems. Somatic nerves mediate voluntary movement. The autonomic nervous system is further subdivided into the sympathetic and the parasympathetic nervous systems. The sympathetic nervous system is activated in cases of emergencies to mobilize energy, while the parasympathetic nervous system is activated when organisms are in a relaxed state. The enteric nervous system functions to control the gastrointestinal system. Both autonomic and enteric nervous systems function involuntarily. Nerves that exit from the cranium are called cranial nerves while those exiting from the spinal cord are called spinal nerves.

<span class="mw-page-title-main">Suprachiasmatic nucleus</span> Part of the brains hypothalamus

The suprachiasmatic nucleus or nuclei (SCN) is a small region of the brain in the hypothalamus, situated directly above the optic chiasm. It is the principle circadian pacemaker in mammals and is necessary for generating circadian rhythms. Reception of light inputs from photosensitive retinal ganglion cells allow the SCN to coordinate the subordinate cellular clocks of the body and entrain to the environment. The neuronal and hormonal activities it generates regulate many different body functions in an approximately 24-hour cycle.

<span class="mw-page-title-main">Motor cortex</span> Region of the cerebral cortex

The motor cortex is the region of the cerebral cortex involved in the planning, control, and execution of voluntary movements. The motor cortex is an area of the frontal lobe located in the posterior precentral gyrus immediately anterior to the central sulcus.

<span class="mw-page-title-main">Neural circuit</span> Network or circuit of neurons

A neural circuit is a population of neurons interconnected by synapses to carry out a specific function when activated. Multiple neural circuits interconnect with one another to form large scale brain networks.

Alpha waves, or the alpha rhythm, are neural oscillations in the frequency range of 8–12 Hz likely originating from the synchronous and coherent electrical activity of thalamic pacemaker cells in humans. Historically, they are also called "Berger's waves" after Hans Berger, who first described them when he invented the EEG in 1924.

Brainwave entrainment, also referred to as brainwave synchronization or neural entrainment, refers to the observation that brainwaves will naturally synchronize to the rhythm of periodic external stimuli, such as flickering lights, speech, music, or tactile stimuli.

Central pattern generators (CPGs) are self-organizing biological neural circuits that produce rhythmic outputs in the absence of rhythmic input. They are the source of the tightly-coupled patterns of neural activity that drive rhythmic and stereotyped motor behaviors like walking, swimming, breathing, or chewing. The ability to function without input from higher brain areas still requires modulatory inputs, and their outputs are not fixed. Flexibility in response to sensory input is a fundamental quality of CPG-driven behavior. To be classified as a rhythmic generator, a CPG requires:

  1. "two or more processes that interact such that each process sequentially increases and decreases, and
  2. that, as a result of this interaction, the system repeatedly returns to its starting condition."
<span class="mw-page-title-main">Neural oscillation</span> Brainwaves, repetitive patterns of neural activity in the central nervous system

Neural oscillations, or brainwaves, are rhythmic or repetitive patterns of neural activity in the central nervous system. Neural tissue can generate oscillatory activity in many ways, driven either by mechanisms within individual neurons or by interactions between neurons. In individual neurons, oscillations can appear either as oscillations in membrane potential or as rhythmic patterns of action potentials, which then produce oscillatory activation of post-synaptic neurons. At the level of neural ensembles, synchronized activity of large numbers of neurons can give rise to macroscopic oscillations, which can be observed in an electroencephalogram. Oscillatory activity in groups of neurons generally arises from feedback connections between the neurons that result in the synchronization of their firing patterns. The interaction between neurons can give rise to oscillations at a different frequency than the firing frequency of individual neurons. A well-known example of macroscopic neural oscillations is alpha activity.

A neuronal ensemble is a population of nervous system cells involved in a particular neural computation.

Theta waves generate the theta rhythm, a neural oscillation in the brain that underlies various aspects of cognition and behavior, including learning, memory, and spatial navigation in many animals. It can be recorded using various electrophysiological methods, such as electroencephalogram (EEG), recorded either from inside the brain or from electrodes attached to the scalp.

<span class="mw-page-title-main">Scratch reflex</span> Response to activation of sensory neurons

The scratch reflex is a response to activation of sensory neurons whose peripheral terminals are located on the surface of the body. Some sensory neurons can be activated by stimulation with an external object such as a parasite on the body surface. Alternatively, some sensory neurons can respond to a chemical stimulus that produces an itch sensation. During a scratch reflex, a nearby limb reaches toward and rubs against the site on the body surface that has been stimulated. The scratch reflex has been extensively studied to understand the functioning of neural networks in vertebrates. Despite decades of research, key aspects of the scratch reflex are still unknown, such as the neural mechanisms by which the reflex is terminated.

The preBötzinger complex, often abbreviated as preBötC, is a functionally and anatomically specialized site in the ventral-lateral region of the lower medulla oblongata. The preBötC is part of the ventral respiratory group of respiratory related interneurons. Its foremost function is to generate the inspiratory breathing rhythm in mammals. In addition, the preBötC is widely and paucisynaptically connected to higher brain centers that regulate arousal and excitability more generally such that respiratory brain function is intimately connected with many other rhythmic and cognitive functions of the brain and central nervous system. Further, the preBötC receives mechanical sensory information from the airways that encode lung volume as well as pH, oxygen, and carbon dioxide content of circulating blood and the cerebrospinal fluid.

Recurrent thalamo-cortical resonance is an observed phenomenon of oscillatory neural activity between the thalamus and various cortical regions of the brain. It is proposed by Rodolfo Llinas and others as a theory for the integration of sensory information into the whole of perception in the brain. Thalamocortical oscillation is proposed to be a mechanism of synchronization between different cortical regions of the brain, a process known as temporal binding. This is possible through the existence of thalamocortical networks, groupings of thalamic and cortical cells that exhibit oscillatory properties.

The trisynaptic circuit, or trisynaptic loop is a relay of synaptic transmission in the hippocampus. The circuit was initially described by the neuroanatomist Santiago Ramon y Cajal, in the early twentieth century, using the Golgi staining method. After the discovery of the trisynaptic circuit, a series of research has been conducted to determine the mechanisms driving this circuit. Today, research is focused on how this loop interacts with other parts of the brain, and how it influences human physiology and behaviour. For example, it has been shown that disruptions within the trisynaptic circuit leads to behavioural changes in rodent and feline models.

The neuroscience of music is the scientific study of brain-based mechanisms involved in the cognitive processes underlying music. These behaviours include music listening, performing, composing, reading, writing, and ancillary activities. It also is increasingly concerned with the brain basis for musical aesthetics and musical emotion. Scientists working in this field may have training in cognitive neuroscience, neurology, neuroanatomy, psychology, music theory, computer science, and other relevant fields.

<span class="mw-page-title-main">Spinal locomotion</span>

Spinal locomotion results from intricate dynamic interactions between a central program in lower thoracolumbar spine and proprioceptive feedback from body in the absence of central control by brain as in complete spinal cord injury (SCI). Following SCI, the spinal circuitry below the lesion site does not become silent rather it continues to maintain active and functional neuronal properties although in a modified manner.

<span class="mw-page-title-main">Neural substrate of locomotor central pattern generators in mammals</span>

Central pattern generators are biological neural networks organized to produce any rhythmic output without requiring a rhythmic input. In mammals, locomotor CPGs are organized in the lumbar and cervical segments of the spinal cord, and are used to control rhythmic muscle output in the arms and legs. Certain areas of the brain initiate the descending neural pathways that ultimately control and modulate the CPG signals. In addition to this direct control, there exist different feedback loops that coordinate the limbs for efficient locomotion and allow for the switching of gaits under appropriate circumstances.

<span class="mw-page-title-main">Neuroscience of sleep</span> Study of the neuroscientific and physiological basis of the nature of sleep

The neuroscience of sleep is the study of the neuroscientific and physiological basis of the nature of sleep and its functions. Traditionally, sleep has been studied as part of psychology and medicine. The study of sleep from a neuroscience perspective grew to prominence with advances in technology and the proliferation of neuroscience research from the second half of the twentieth century.

In the field of chronobiology, the dual circadian oscillator model refers to a model of entrainment initially proposed by Colin Pittendrigh and Serge Daan. The dual oscillator model suggests the presence of two coupled circadian oscillators: E (evening) and M (morning). The E oscillator is responsible for entraining the organism’s evening activity to dusk cues when the daylight fades, while the M oscillator is responsible for entraining the organism’s morning activity to dawn cues, when daylight increases. The E and M oscillators operate in an antiphase relationship. As the timing of the sun's position fluctuates over the course of the year, the oscillators' periods adjust accordingly. Other oscillators, including seasonal oscillators, have been found to work in conjunction with circadian oscillators in order to time different behaviors in organisms such as fruit flies.

References

  1. 1 2 3 4 5 6 7 8 9 10 Buzsáki, G (2006). The Rhythms of the Brain. Oxford Press.
  2. ↑ Purves, Dale (2012). Neuroscience. Vol. V. Sinauer Associates, INC. pp. 628–636.
  3. 1 2 Hooper, Scott L. (1999–2010). "Central Pattern Generators". Encyclopedia of Life Sciences. John Wiley & Sons. doi:10.1038/npg.els.0000032. ISBN   978-0-470-01590-2.
  4. ↑ Calancie B, Needham-Shropshire B, Jacobs P, Willer K, Zych G, Green BA (October 1994). "Involuntary stepping after chronic spinal cord injury. Evidence for a central rhythm generator for locomotion in man". Brain. 117 (Pt 5): 1143–59. doi:10.1093/brain/117.5.1143. PMID   7953595.
  5. ↑ Richter, D.W. (1996). "Neural regulation of Respiration: Rhythmogenesis and Afferent control". Comprehensive Human Physiology. Vol. 2. pp. 2079–2095. doi:10.1007/978-3-642-60946-6_106. ISBN   978-3-642-64619-5.{{cite book}}: Missing or empty |title= (help)
  6. ↑ Handel, Stephen (1989). Listening: An introduction to the perception of auditory events. MIT Press.
  7. ↑ Smith, Roger and Bradley, Efron (1997). "Circadian Rhythm and Enhances Athletic Performance in the National Football League". Sleep. 20 (5): 362–365. PMID   9381059.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  8. ↑ Kline, CE (2007). "Circadian variation in swim performance". Journal of Applied Physiology. 102 (2): 641–649. doi:10.1152/japplphysiol.00910.2006. PMID   17095634. S2CID   2935066.
  9. ↑ Brain Beats
  10. ↑ "Dueling Banjos"
  11. ↑ Grahn, Jessica & Brett, Matthew (2007). "Rhythm and Beat Perception in Motor Areas of the Brain". Journal of Cognitive Neuroscience. 19 (5): 893–906. CiteSeerX   10.1.1.119.5718 . doi:10.1162/jocn.2007.19.5.893. PMID   17488212. S2CID   5992236.
  12. ↑ Trappenberg, Thomas P (2002). The Fundamentals of Computational Neurosciences. Oxford Press.
  13. ↑ Doya, Kenji & Terrence J. Sejnowski (1999). The New Cognitive Neurosciences. Vol. II. MIT Press. pp. 469–482.
  14. ↑ Sober, Sam; Brainard, Michael (2009). "Adult Birdsong Is Actively Maintained by Error Correction". Nature Neuroscience. 12 (7): 927–931. doi:10.1038/nn.2336. PMC   2701972 . PMID   19525945.
  15. ↑ Conway, B.A. (1995). "Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man". Journal of Physiology. 489 (3): 917–924. doi:10.1113/jphysiol.1995.sp021104. PMC   1156860 . PMID   8788955.
  16. ↑ Salenius, S. (1997). "Cortical control of human motoneuron firing during isometric contraction". Journal of Neurophysiology. 77 (6): 3401–3405. doi:10.1152/jn.1997.77.6.3401. PMID   9212286.
  17. ↑ Haliday, D.M. (1998). "Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans". Neuroscience Letters. 241 (1): 5–8. doi:10.1016/s0304-3940(97)00964-6. PMID   9502202. S2CID   12959403.
  18. ↑ Baker, S.M. (1997). "Coherent oscillations in monkey motor cortex and hand muscle EMG show task dependent modulation". Journal of Physiology. 501 (Pt 1): 225–241. doi:10.1111/j.1469-7793.1997.225bo.x. PMC   1159515 . PMID   9175005.
  19. ↑ Kilner, J.M. (1999). "Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles". Journal of Physiology. 516 (2): 559–570. doi:10.1111/j.1469-7793.1999.0559v.x. PMC   2269269 . PMID   10087353.
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