Cutaneous reflex in human locomotion
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Cutaneous Skin is the layer of usually soft, flexible outer tissue covering the body of a vertebrate animal, with three main functions: protection, regulation, and sensation. Other animal coverings, such as the arthropod exoskeleton, have different de ...
, superficial, or skin
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
es, are activated by skin receptors and play a valuable role in
locomotion Locomotion means the act or ability of something to transport or move itself from place to place. Locomotion may refer to: Motion * Motion (physics) * Robot locomotion, of man-made devices By environment * Aquatic locomotion * Flight * Locomo ...
, providing quick responses to unexpected environmental challenges. They have been shown to be important in responses to obstacles or stumbling, in preparing for visually challenging terrain, and for assistance in making adjustments when instability is introduced. In addition to the role in normal locomotion, cutaneous reflexes are being studied for their potential in enhancing rehabilitation therapy (
physiotherapy Physical therapy (PT), also known as physiotherapy, is one of the allied health professions. It is provided by physical therapists who promote, maintain, or restore health through physical examination, diagnosis, management, prognosis, patient ...
) for people with
gait abnormalities Gait is the pattern of movement of the limbs of animals, including humans, during locomotion over a solid substrate. Most animals use a variety of gaits, selecting gait based on speed, terrain, the need to maneuver, and energetic efficiency. Di ...
.


Background of reflex pathway

Reflexes In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a Stimulus (physiology), stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous s ...
are a vital part of our everyday activities. We have all experienced how fast and automatic these responses to environmental interactions can be. They can protect us from potentially dangerous situations such as touching a hot stove or stepping on a tack. There are also
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
pathways involved in more dynamic activities such as walking and running, helping to ensure a smooth
gait Gait is the pattern of movement of the limbs of animals, including humans, during locomotion over a solid substrate. Most animals use a variety of gaits, selecting gait based on speed, terrain, the need to maneuver, and energetic efficiency. Di ...
and allowing us to respond quickly to obstacles or unexpected perturbations or disturbances. The reflex pathway (
reflex arc A reflex arc is a neural pathway that controls a reflex. In vertebrates, most sensory neurons do not pass directly into the brain, but synapse in the spinal cord. This allows for faster reflex actions to occur by activating spinal motor neurons w ...
) is a sequence of
neurons A neuron, neurone, or nerve cell is an electrically excitable cell that communicates with other cells via specialized connections called synapses. The neuron is the main component of nervous tissue in all animals except sponges and placozoa. N ...
connecting the sensory input (
afferent neuron Afferent nerve fibers are the axons (nerve fibers) carried by a sensory nerve that relay sensory information from sensory receptors to regions of the brain. Afferent projections ''arrive'' at a particular brain region. Efferent nerve fibers a ...
) to the motor output (
efferent neuron Efferent nerve fibers refer to axonal projections that ''exit'' a particular region; as opposed to afferent projections that ''arrive'' at the region. These terms have a slightly different meaning in the context of the peripheral nervous syste ...
), resulting in a behavioral response. The general pathway of a spinal reflex is one which involves neurons contained within the
spinal cord The spinal cord is a long, thin, tubular structure made up of nervous tissue, which extends from the medulla oblongata in the brainstem to the lumbar region of the vertebral column (backbone). The backbone encloses the central canal of the spi ...
. However, the
brain 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 v ...
may also provide additional ( supraspinal) contributions, which can modulate the responsiveness of the reflex to the sensory input.


General reflex pathways

Reflexes can be very simple, as in the monosynaptic
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
, which only contains one
synapse In the nervous system, a synapse is a structure that permits a neuron (or nerve cell) to pass an electrical or chemical signal to another neuron or to the target effector cell. Synapses are essential to the transmission of nervous impulses from ...
, or more complicated, as in the polysynaptic
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
, which involves more than one
synapse In the nervous system, a synapse is a structure that permits a neuron (or nerve cell) to pass an electrical or chemical signal to another neuron or to the target effector cell. Synapses are essential to the transmission of nervous impulses from ...
. The
knee jerk The patellar reflex, also called the knee reflex or knee-jerk, is a stretch reflex which tests the L2, L3, and L4 segments of the spinal cord. Mechanism Striking of the patellar tendon with a reflex hammer just below the patella stretches the mus ...
reflex is a common example of a monosynaptic reflex when one is looking at the
quadriceps The quadriceps femoris muscle (, also called the quadriceps extensor, quadriceps or quads) is a large muscle group that includes the four prevailing muscles on the front of the thigh. It is the sole extensor muscle of the knee, forming a large ...
motor response of kicking your leg out. It can also be used as an example of a polysynaptic reflex when looking at the involvement of inhibitory interneurons to relax the
hamstring In human anatomy, a hamstring () is any one of the three posterior thigh muscles in between the hip and the knee (from medial to lateral: semimembranosus, semitendinosus and biceps femoris). The hamstrings are susceptible to injury. In quadrupeds, ...
s. The complexity of the reflex can be estimated by examining the time delay, or latency, between the electrical stimulation of the sensory neuron and the corresponding motor response, as measured by EMG (
electromyography Electromyography (EMG) is a technique for evaluating and recording the electrical activity produced by skeletal muscles. EMG is performed using an instrument called an electromyograph to produce a record called an electromyogram. An electromyog ...
). Most reflexes can be categorized in one of three groups depending on the latency of EMG response. The short-latency reflex (SLR) is the fastest (~40-50 ms) and involves a mono-synaptic pathway. The medium-latency reflex (MLR) utilizes
interneurons Interneurons (also called internuncial neurons, relay neurons, association neurons, connector neurons, intermediate neurons or local circuit neurons) are neurons that connect two brain regions, i.e. not direct motor neurons or sensory neurons. In ...
within the spinal cord and is typically ~80-90 ms. The long-latency reflex (LLR) is ~120-140 ms, suggesting that it is mediated by additional supraspinal input from the brain.


Cutaneous receptors and reflexes

Cutaneous receptors A cutaneous receptor is the type of sensory receptor found in the skin ( the dermis or epidermis). They are a part of the somatosensory system. Cutaneous receptors include mechanoreceptors (pressure or distortion), nociceptors (pain), and th ...
are a type of
sensory receptor Sensory neurons, also known as afferent neurons, are neurons in the nervous system, that convert a specific type of stimulus, via their receptors, into action potentials or graded potentials. This process is called sensory transduction. The cell ...
, which respond to stimuli (touch, pressure, pain, temperature) that provide information regarding contact with the external environment. A common
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
involving cutaneous receptors is the
crossed extensor reflex The crossed extensor reflex or crossed extensor response or crossed extension reflex is a reflex in which the contralateral limb compensates for loss of support when the ipsilateral limb withdraws from painful stimulus in a withdrawal reflex. Dur ...
. This reflex is recruited when we experience a painful stimulus on the bottom of our foot, such as stepping on a tack. The response is to quickly pull the foot that stepped on the tack away, and at the same time, shift our weight to the opposite (
contralateral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position prov ...
) leg for balance. It has been noted that the muscle activation response to cutaneous receptor stimulation can be modulated by a variety of factors. These include the: * cutaneous nerve stimulated * phase of the gait cycle * intensity of the stimulation * nature of the task being performed * rhythmic arm or leg movements * complexity of the task. In addition to modulation, the cutaneous reflex has been shown to evoke both a MLR (medium latency response) and LLR (long latency response) EMG response, indicating that it is a polysynaptic
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
, involving spinal
interneurons Interneurons (also called internuncial neurons, relay neurons, association neurons, connector neurons, intermediate neurons or local circuit neurons) are neurons that connect two brain regions, i.e. not direct motor neurons or sensory neurons. In ...
or supraspinal pathways


Functional role

The cutaneous reflex has been attributed to functional responses to disturbances encountered during locomotion and is, therefore, dependent on which cutaneous nerve is stimulated. Examples of nerves whose cutaneous branches have been examined are the: 1.
Superficial fibular nerve The superficial fibular nerve (also known as superficial peroneal nerve) innervates the fibularis longus and fibularis brevis muscles and the skin over the antero-lateral aspect of the leg along with the greater part of the dorsum of the foot (wit ...
or
peroneal nerve The common fibular nerve (also known as the common peroneal nerve, external popliteal nerve, or lateral popliteal nerve) is a nerve in the lower leg that provides sensation over the posterolateral part of the leg and the knee joint. It divides at ...
(innervating the dorsal aspect of the foot) 2.
Tibial nerve The tibial nerve is a branch of the sciatic nerve. The tibial nerve passes through the popliteal fossa to pass below the arch of soleus. Structure Popliteal fossa The tibial nerve is the larger terminal branch of the sciatic nerve with root val ...
(innervating the plantar surface of the foot)3.
Sural nerve The sural nerve ''(L4-S1)'' is generally considered a pure cutaneous nerve of the posterolateral leg to the lateral ankle. The sural nerve originates from a combination of either the sural communicating branch and medial sural cutaneous nerve, or ...
(innervating the lateral portion of the foot)4.
Superficial branch of radial nerve The superficial branch of the radial nerve passes along the front of the radial side of the forearm to the commencement of its lower third. It is a sensory nerve. It lies at first slightly lateral to the radial artery, concealed beneath the Brac ...
(innervating forearm and hand on the thumb side) Human locomotion is often examined from the perspective of the gait cycle. Cutaneous reflexes demonstrate variations in the muscles activated and the timing at which they are activated depending on which portion of the gait cycle the stimulation occurs. This variation suggests a functional role for the reflex to provide us with a smooth gait alteration when encountering or anticipating obstacles and challenging terrain. The major muscles impacted involve four (4) motions important to locomotion:


Superficial fibular nerve (SF)

Cutaneous stimulation of the
superficial fibular nerve The superficial fibular nerve (also known as superficial peroneal nerve) innervates the fibularis longus and fibularis brevis muscles and the skin over the antero-lateral aspect of the leg along with the greater part of the dorsum of the foot (wit ...
(SF) would typically occur when the top of the foot encounters an obstacle. The reflexive response to this activation is to pull the leg up and over the obstacle, while also preparing for a possible stumble or fall. Observed EMG muscle responses to SF stimulation help to explain how this reflexive response is accomplished: * Increased biceps femoris activity flexes the knee, pulling the leg up and over the obstacle. * Decreased tibialis anterior activity allows the gastrocnemius to more completely plantar flex, or point the toe. This allows the foot to slide over the obstacle. * Increased vastus lateralis activity produces a co-contraction of the hamstrings and quadriceps, which provides increased knee stability in case of a stumble or fall.


Tibial nerve (TN)

Tibial nerve The tibial nerve is a branch of the sciatic nerve. The tibial nerve passes through the popliteal fossa to pass below the arch of soleus. Structure Popliteal fossa The tibial nerve is the larger terminal branch of the sciatic nerve with root val ...
(TN) stimulation demonstrates a phase dependent response, in which the muscle activation varies depending on what part of the gait cycle a person is in when the stimulation occurs. 1. In normal, unimpeded walking, TN activation during the transition from stance to swing should decrease as the foot begins to leave the ground. In this case, increased TN stimulation would suggest scuffing of the bottom of the foot along the ground. The reflexive response will bring the foot up, pulling it off the ground. EMG responses to stimulation, again, help to explain how this is accomplished. * Increased tibialis anterior activity produces dorsiflexion, raising the foot off the ground. 2. TN activation during late swing in normal walking should begin to increase as the foot begins to contact the ground. TN stimulation during this phase is, therefore, similar to a normal gait pattern sensory input. In this situation, the foot will plantar flex to allow smooth placement for the transition to the stance phase. Here, the opposite EMG effect is observed. * Decreased tibialis anterior activity reduces active dorsiflexion, allowing the ankle to achieve greater plantar flexion.


Sural nerve (SN)

Sural nerve The sural nerve ''(L4-S1)'' is generally considered a pure cutaneous nerve of the posterolateral leg to the lateral ankle. The sural nerve originates from a combination of either the sural communicating branch and medial sural cutaneous nerve, or ...
(SN) stimulation results in a reflex that is both phase and intensity dependent. The sural nerve innervates the lateral (outside) portion of the foot and could be activated during either the swing or stance phase when encountering uneven terrain. The intensity dependent response is indicative of the level of activation and, therefore, the potential for harm. 1. During the swing phase, SN stimulation indicates encountering an obstacle on the lateral side of the foot. The reaction is to move the foot inward and the leg up, out of the way. Observed EMG responses are: * Increased tibialis anterior activity to cause dorsiflexion and inversion (turning the foot inward) of the foot. * Increased biceps femoris activity will cause knee flexion to raise the foot higher and away from the obstacle. * Decreased vastus lateralis activity will increase the ability for the biceps femoris to flex the knee to pull it up. 2. During the stance phase, a moderate intensity SN stimulation is indicative of uneven terrain and will result in a response that provides stiffness and stability to the ankle. The mechanism for this response is accomplished through the simultaneous activation of two antagonistic ankle muscles * Increased gastrocnemius and tibialis anterior activity will provide stiffness to the ankle joint, helping to prevent the spraining of the ankle. 3. During the stance phase, a high intensity SN stimulation is indicative of an obstacle that could potentially cause physical damage to the foot. In this case, the goal of the reflex would be to remove the foot completely away from the stimulus. * Decreased activity of the gastrocnemius will allow for a more complete dorsiflexion and inversion by the tibialis anterior pulling the foot both up and inward, preventing the foot from staying in contact with the potentially damaging surface.


Superficial radial nerve (SR)

Cutaneous stimulation of the superficial
radial nerve The radial nerve is a nerve in the human body that supplies the posterior portion of the upper limb. It innervates the medial and lateral heads of the triceps brachii muscle of the arm, as well as all 12 muscles in the posterior osteofascial comp ...
(located on the thumb side of the forearm) will evoke a cutaneous reflex in arm muscles during rhythmic arm movements in a manner similar to that observed with leg muscles during
locomotion Locomotion means the act or ability of something to transport or move itself from place to place. Locomotion may refer to: Motion * Motion (physics) * Robot locomotion, of man-made devices By environment * Aquatic locomotion * Flight * Locomo ...
. In addition to its role in reflex responses to the arm itself, it will modulate leg muscle cutaneous reflexes during locomotion. This reflexive response may be a vestigial remnant from our
quadruped Quadrupedalism is a form of locomotion where four limbs are used to bear weight and move around. An animal or machine that usually maintains a four-legged posture and moves using all four limbs is said to be a quadruped (from Latin ''quattuor' ...
ancestry, connecting
forelimb A forelimb or front limb is one of the paired articulated appendages (limbs) attached on the cranial ( anterior) end of a terrestrial tetrapod vertebrate's torso. With reference to quadrupeds, the term foreleg or front leg is often used instead. ...
movement with
hindlimb A hindlimb or back limb is one of the paired articulated appendages (limbs) attached on the caudal ( posterior) end of a terrestrial tetrapod vertebrate's torso.http://www.merriam-webster.com/medical/hind%20limb, Merriam Webster Dictionary-Hindl ...
movement. This connection can be seen with normal walking, when the arm swings in rhythm with the opposite leg. The crossed synchrony may be partially due to a shared
neural pathway In neuroanatomy, a neural pathway is the connection formed by axons that project from neurons to make synapses onto neurons in another location, to enable neurotransmission (the sending of a signal from one region of the nervous system to an ...
between upper and lower limbs. While the function of this coordinated movement may be involved in maintaining balance while shifting our center of mass, it is also involved in locomotive reflexes. Stimulation of the radial nerve during walking is unusual and often indicative of an obstacle that is high enough to make contact with the swinging arm. Concurrent, or simultaneous stimulation of both the superficial fibular nerve (top of the foot) and the superficial radial nerve of the opposite (
contralateral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position prov ...
) arm suggests that the obstacle is large enough to cause a major stumble or fall. The response is, therefore, one which activates the leg muscles in a way as to prepare for that possibility. EMG responses to this type of simultaneous stimulation involves significant changes in the leg opposite or (
contralateral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position prov ...
) to the side receiving the radial simulation: * Increased activity of the contralateral tibialis anterior and contralateral vastus lateralis to provide additional stiffness and stability to the leg.


Additional variables modulating cutaneous reflex response

The magnitude of the
cutaneous Skin is the layer of usually soft, flexible outer tissue covering the body of a vertebrate animal, with three main functions: protection, regulation, and sensation. Other animal coverings, such as the arthropod exoskeleton, have different de ...
reflex in leg muscles can be altered by multiple variables. The alterations are movement dependent, gait phase dependent, and can be either
excitatory In neuroscience, an excitatory postsynaptic potential (EPSP) is a postsynaptic potential that makes the postsynaptic neuron more likely to fire an action potential. This temporary depolarization of postsynaptic membrane potential, caused by the ...
or
inhibitory An inhibitory postsynaptic potential (IPSP) is a kind of synaptic potential that makes a postsynaptic neuron less likely to generate an action potential.Purves et al. Neuroscience. 4th ed. Sunderland (MA): Sinauer Associates, Incorporated; 2008. ...
to the normal cutaneous
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
pattern.


Complexity or challenge of the task

Cutaneous reflexes are modulated in conditions which present
instability In numerous fields of study, the component of instability within a system is generally characterized by some of the outputs or internal states growing without bounds. Not all systems that are not stable are unstable; systems can also be mar ...
or challenging locomotive movements. In unstable conditions, such as disturbances occurring when the arms are crossed, there is facilitation or amplification in both the
ipsilateral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position pro ...
and
contralateral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position prov ...
reflexes which are muscle specific. With
superficial fibular nerve The superficial fibular nerve (also known as superficial peroneal nerve) innervates the fibularis longus and fibularis brevis muscles and the skin over the antero-lateral aspect of the leg along with the greater part of the dorsum of the foot (wit ...
stimulation, the ipsilateral
biceps femoris The biceps femoris () is a muscle of the thigh located to the posterior, or back. As its name implies, it has two parts, one of which (the long head) forms part of the hamstrings muscle group. Structure It has two heads of origin: *the ''long h ...
(knee flexor) and ipsilateral
soleus In humans and some other mammals, the soleus is a powerful muscle in the back part of the lower leg (the calf). It runs from just below the knee to the heel, and is involved in standing and walking. It is closely connected to the gastrocnemius mu ...
(plantar flexor) reflexes are amplified during swing to allow the leg to clear the obstacle. In contrast, the contralateral, opposite, leg demonstrates amplification of both the
tibialis anterior The tibialis anterior muscle is a muscle in humans that originates along the upper two-thirds of the lateral (outside) surface of the tibia and inserts into the medial cuneiform and first metatarsal bones of the foot. It acts to dorsiflex and inve ...
(dorsiflexor) and the
gastrocnemius The gastrocnemius muscle (plural ''gastrocnemii'') is a superficial two-headed muscle that is in the back part of the lower leg of humans. It runs from its two heads just above the knee to the heel, a three joint muscle (knee, ankle and subtalar ...
(plantar flexor) providing additional leg stiffness for stability of the stance leg. Similar amplification results are seen in both visually challenging environments, such as horizontal ladder stepping, and backward walking. These situations demonstrate facilitation of the contralateral reflexes during the stance phase to in a manner which would provide stability and ipsilateral reflex modulation in a way to allow smooth transition past the perceived obstacle.


Potential clinical applications of cutaneous reflex modulation

The ability to modulate the magnitude of cutaneous reflexes via rhythmic arm movements or challenging environments has potential implications in rehabilitation for patients with motor weakness. Some
stroke A stroke is a medical condition in which poor blood flow to the brain causes cell death. There are two main types of stroke: ischemic, due to lack of blood flow, and hemorrhagic, due to bleeding. Both cause parts of the brain to stop functionin ...
patients with lower limb complications demonstrate reduced or blunted
cutaneous Skin is the layer of usually soft, flexible outer tissue covering the body of a vertebrate animal, with three main functions: protection, regulation, and sensation. Other animal coverings, such as the arthropod exoskeleton, have different de ...
reflexes. These lower limb
reflex In biology, a reflex, or reflex action, is an involuntary, unplanned sequence or action and nearly instantaneous response to a stimulus. Reflexes are found with varying levels of complexity in organisms with a nervous system. A reflex occurs ...
es can be amplified with superficial
radial nerve The radial nerve is a nerve in the human body that supplies the posterior portion of the upper limb. It innervates the medial and lateral heads of the triceps brachii muscle of the arm, as well as all 12 muscles in the posterior osteofascial comp ...
stimulation by taking advantage of the interlimb reflex observed during rhythmic arm locomotion between the upper and lower limbs. The amplification of the
contralateral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position prov ...
tibialis anterior The tibialis anterior muscle is a muscle in humans that originates along the upper two-thirds of the lateral (outside) surface of the tibia and inserts into the medial cuneiform and first metatarsal bones of the foot. It acts to dorsiflex and inve ...
seen during the swing to stance transition may be clinically useful in preventing
foot drop Foot drop is a gait abnormality in which the dropping of the forefoot happens due to weakness, irritation or damage to the deep fibular nerve (deep peroneal), including the sciatic nerve, or paralysis of the muscles in the anterior portion of t ...
during the swing phase for stroke patients.Zehr, E. P., & Loadman, P. M. (2012). Persistence of locomotor-related interlimb reflex networks during walking after stroke. Clinical Neurophysiology, 123(4), 796-807. Future research is needed to further explore the efficacy of cutaneous reflex amplification for as a tool for enhancing motor receptivity with stroke rehabilitation.


External links


Video example of the Stumble Response in NYCGait AnalysisInterlimb Coordination of LocomotionUpper limb reflexes in rehabilitation


References

{{reflist Reflexes