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Stretch Receptor: A Model for Muscle Spindle Organs

Introduction

To coordinate movements, a nervous system must monitor the positions and movements of body parts. This is done with movement- and position-sensitive receptors called proprioceptors. Some of these are stretch-sensitive receptors embedded in or parallel to muscle fibers. The muscle spindle organs of humans belong to this class of proprioceptors, as do the muscle receptor organs (MROs) of crustaceans. In each case, the sensory organ reports position and helps guide body movements (part of the kinesthetic sense). Proprioceptors are one type of somatic receptor (Hill et al., 2012; Purves et al., 2013; Silverthorn, 2013). The two other types are exteroceptors, which contribute to tactile, thermal, and pain sensation, and enteroceptors, which regulate breathing, thirst, hunger, and blood pressure. Many somatic receptors have similar mechanisms for transducing stimulus energy into a neural response.

There are two types of MROs in crustaceans, slow-adapting and fast-adapting. Each superficial extensor muscle (Figure A.1) has one MRO of each type associated with it. There is a superficial extensor muscle on each side of each abdominal segment and in the two most posterior thoracic segments. The superficial extensor muscles span adjacent segments, running from the middle of one tergite to the back edge of the next most anterior tergite. When these muscles contract, they pull the tergites together, causing the abdomen to straighten and extend (thus the name). Conversely, when the abdomen is curled ventrally, the tergites rotate around their joints and the extensor muscles are stretched, along with their associated MROs (Figure 7.1).

Each MRO is composed of a sensory neuron and its associated muscle. RM1 is the muscle with the slow-adapting receptor (MRO1); RM2 is the muscle with the fast-adapting receptor (MRO2). Each MRO muscle has the dendrites of a sensory neuron embedded in it. The axons of the two MROs travel together from their dorsal muscles, laterally around the large abdominal muscles, to the ventral nerve cord to enter the abdominal ganglia as part of the second ganglionic nerve (nerve 2).

The receptor muscles have excitatory motor innervation in parallel with that of the dorsal extensor muscles and contract in unison with the extensor muscles. The receptor muscles are thus similar to other muscles except for the associated receptor neuron. This arrangement also occurs in the muscle spindle organs of human skeletal muscles. Both MRO neurons receive inhibitory synaptic innervation from the central ganglion (this does not occur in vertebrate proprioceptors). These inhibitory inputs depress the receptor activity.

The crustacean stretch receptor is one of the classic model preparations of neurophysiology (Purali, 2005; Rydqvist et al., 2007). It has been used to examine basic properties of sensory function such as the generator potential, spike initiation, efferent control, and sensory adaptation, as well as neural integration since it receives direct inhibitory input.

In this lab exercise, you will record extracellularly from the nerve that carries sensory information from the MROs to the central nervous system while curling the tail to stimulate these receptors. This recording will allow you to determine the stimulus-response properties of the MROs and measure the adaptation rate of the MROs. You will observe some basic features of sensory systems in this exercise, including adequate stimuli, adaptation, and range fractionation.

Dissection

Look at a methylene blue−stained specimen before starting. This specimen shows broken branches of nerve 2 leaving the receptor muscles at the sides of the dorsal abdomen. The stained preparation will help you see what you are trying to achieve in the dissection.

Recording

Experiments

Stimulus-Response Properties of MRO1

Using the manipulator, slowly curl the abdomen and observe action potentials in the nerve. Increase the stretch. How does this affect the frequency of action potentials? The activity you see is from the slow-adapting receptor, MRO1. Relax the tail just to the point at which MRO1 is no longer active and designate this as zero stretch. Curl it again by a measured amount (using the scale on the manipulator). Measure the maximal response (number of action potentials per unit time, maybe the first 5 s). Relax the tail again and repeat with a different amount of stretch. Measure the maximal response with several different amounts of stretch and graph the relationship between maximal response and units of stretch. (See the next section for an alternate way of quantifying the response.)

Adaptation of MRO1

In the previous experiment, you probably noticed that the receptor was most active just after the full stretch was achieved and that action potential firing then slowed down. This slowing is due to receptor adaptation, a basic feature of sensory systems. Quantify adaptation by recording 30 s of the response to a sustained stretch. Graph the instantaneous firing rate vs. time. How rapidly does the firing rate decrease? Try fitting an exponential equation to it, starting the fit where the frequency reaches its maximum. Does adaptation rate vary with the amount of stretch? Appendix E, Analysis Tools, can find the instantaneous firing rate and fit the exponential equation for you. (Ask your instructor how to copy waveform data from your data-acquisition software into the analysis tools.)

If you do exponential fits of firing frequency at several different amounts of stretch, you will get a series of equations of the form:
Rt = R + R0e−t/τ
where Rt is the firing rate at time t, R is the calculated firing rate if this degree of stretch were maintained infinitely, R + R0 is the peak firing rate at time 0, and τ is the adaptation rate. In addition to noting the adaptation rate at each level of stretch, try plotting R vs. stretch. Does this give the same shape of curve as plotting maximum spike rate vs. stretch?

Two Receptor Types

After collecting a complete data set showing adaptation, apply a moderate amount of curl to the tail and then tap the thread lightly to give a sudden brief stretch (Video 7.8, Stimulating MRO2). What happens? You may see two sizes of action potential in response to this stimulus. The smaller one is MRO1; the larger one that fired only with the sudden stimulus is MRO2. Take care that the preparation does not move too much when you tap. This could cause movement artifacts due to the electrode changing its position on the nerve, which could be mistaken for a response of MRO2. (If you cannot get MRO2 to respond, you may try another segment if there is time.) Try to quantify the adaptation rate of MRO2. This is often difficult because MRO2 adapts so much more quickly than MRO1. Also note what happens to MRO1 during and immediately after sudden stretches. What do these results suggest about the functions of the two receptors?

Further Exploration

The three experiments you performed in this lab showed some of the basic properties of the muscle receptor organs but they should also raise more questions. Many of these can be investigated using the equipment available in your lab. For example, what does the stimulus-response graph look like if the tail is stretched to a point, allowed to adapt, and then stretched further? Does it make a difference how quickly the tail is stretched? How long does adaptation last? If the tail is stretched, allowed to adapt, relaxed, and stretched again, does it reach the same amount of activity as before? Does it adapt at the same rate the second time? How does changing ion concentrations in the saline effect the response to stretch and the adaptation rate? How are these affected by adding the inhibitory transmitter GABA or neuromodulators such as serotonin, or by changing the temperature of the saline bath?

Lab Cleanup

Clean up any spilled saline and rinse the ground electrode with distilled water. Expel saline from the suction electrode and rinse it with distilled water. Put the crayfish tail in the freezer along with the frozen heads and rinse the dissecting dish with fresh water.

Questions

  1. Make a graph of MRO1 response magnitude as a function of stimulus magnitude. Describe the shape of this curve. How does MRO1 appear to code stimulus intensity in its neural response? Any linear part of the curve is called the dynamic response range of the receptor. What is the functional significance of this? What is the significance of any parts of the curve where the response does not increase linearly with stretch?
  2. The “adequate stimulus” is the form of physical energy that has the lowest threshold for receptor activation. Stretching causes action potential firing in MROs by deforming the dendritic membranes of the MRO sensory neuron. Thus membrane deformation is the adequate stimulus for the MRO. This is also the cause of responses in somatic receptors of touch and pressure and of the receptors (hair cells) for hearing. How can deformation of a membrane cause a neural response? What are the adequate stimuli for visual and olfactory receptors? How does the mechanism of signal transduction in the MROs compare to the mechanisms at work in other senses such as vision and olfaction?
  3. Describe the adaptation curve from MRO1 for the response to a single sustained stretch. Does the decay of spike frequency fall linearly or exponentially with time? When was adaptation fastest? How does adaptation rate vary with the amount of stretch? Suggest a cellular mechanism for adaptation of MRO1. Why is it useful for a sensory system to show adaptation? Give an example of yourself experiencing sensory adaptation today.
  4. What different information might the fast-adapting and slow-adapting MROs provide for movement control? How are these two receptor types exhibiting range fractionation? What cellular mechanisms might cause the two receptors to adapt at different rates?
  5. Would you expect temperature changes or neuromodulators to alter the responses of sensory systems? Explain why or why not.
  6. Speculate on the role of the MROs in crayfish behavior (see McCarthy and Macmillan, 1995, 1999; Patullo et al., 2001; Faulkes and Macmillan 2002).
  7. The crayfish MRO differs from vertebrate proprioceptors by having inhibitory input at the receptor level. When might it be useful to have inhibitory input to a sensory receptor? How do vertebrates accomplish inhibition of sensory information without peripheral inhibition?
  8. Proprioceptors are essential for motor control. They provide the feedback necessary for all aspects of motor responses, including movement. Can you imagine moving around your world without proprioceptors? Suggest alternative ways of controlling your movements if your proprioceptors were to stop working one day (Sacks, 1990).

References