JOURNALOF NEUROPHYSIOLOGY Vol. 41, No. 1, January 1978. Printed
in U.S.A.
Synaptic Connectivity in a Crayfish Neuromuscular System. II. Nerve-Muscle Matching and Nerve Branching Patterns SAMUEL Department
SUMMARY
J. VELEZ
AND
of Biology,
AND
ROBERT J. WYMAN Yale University,
New Haven,
CONCLUSIONS
I. In the crayfish slowflexor muscle,the input resistance,time constant, resting potential, and size of the muscle fibers change continuously with position from one edgeof the musclesheet to the other. These properties are possibly indications of the relative “slowness” or “fastness” of the musclefibers. 2. The most tonically firing axon (axon 2) innervates preferentially the medial part of the musclewith the “slower” fibers. Its innervation decreasescontinuously in the lateral direction. The fibers innervated by axon 2 do not show a marked position dependence of the measured characteristics. The most phasic axon (axon 6) with the largest (facilitated) junctional potentials (jp’s) innervates in the oppositedirection, innervating mostly “faster” fibers. The fibers innervated by axon 6 do not show a marked position dependenceof their measuredcharacteristics. 3. Most fibers were either innervated by 2 and not by 6, or were innervated by 6 but not by 2. The percentage of fibers belonging to the two groups varies continuously across the muscle, explaining the continuous change in musclefiber characteristic with position. 4. Axons 2 and 6 do not selectively avoid innervating the samefiber. The probability of innervation by both axons in a given region was the product of the probability of innervation by each axon alone for that region. Fibers innervated by both axons had intermediatephysiological characteristics. 5. We proposethat the position of the muscle fiber has no influence, per se, on its differentiation. The mosttonic and most phasicaxons have a trophic or activity-dependent effect, which is responsiblefor the varying musclefiber characteristics. The gradation in muscle fiber properties, then, is due to the gradation of innervation. Received for publication April 2, 1976.
Connecticut
06520
6. Scanning electron micrographswere used to study the branching pattern of the nerve into the muscle. In general, the nerve and its branches run in a medial to lateral direction, but branchescome off at any angle to the main nerve. Branch points appearrandomly scattered over the musclesheetexcept for one prominent backward branch, which always occurs near the middle of the muscle. Comparing right and left sidesof the same animal, there are differences both in the number and location of branches.Comparisonsof the samesidein different animals show roughly comparable dissimilarities. The growth path of the nerve, especially its major backward branch, cannot be explained by a simple growth up or down a gradient. INTRODUCTION
In many animals,vertebrate and invertebrate, there is a “match” between the physiological properties of the muscle fibers and those of the motoneurons which innervate them. This is well documented in mammals, where fast and slow muscle fibers have their corresponding innervation from larger and smalleraxons, respectively (8). In crustaceansthere is also a similar type of matching. Animals have separate phasic and tonic muscles(1). The phasicmuscleshave short sarcomere, rapidly contracting muscle fibers which are driven by phasically firing axons. The tonic muscleshave long sarcomere,slowly contracting fibers driven by tonically firing axons (3). Mixed musclesalsooccur with both types of musclefibers. Somedetailed studies have been made on these mixed musclesand, indeed, in the case where only two axons innervate the muscle fibers, the phasic axon innervates most heavily the short sarcomerefibers of the muscle, while the more tonic axon innervates most heavily the longer sarcomere,slowerfibers(1,2). The superficial flexor muscle of the crayfish 85
Downloaded from www.physiology.org/journal/jn by ${individualUser.givenNames} ${individualUser.surname} (129.059.095.115) on January 13, 2019
86
S. J. VGLEZ
AND
abdomen is a planar sheet of about 40 fibers. The muscle fibers are all of a generally slow type: they have long sarcomere lengths averaging lo- 12 pm and generally exhibit only graded tension changes achieved through summation or facilitation of excitatory junctional potentials (jp’s) (11). This contrasts to the fibers of the synergistic deep flexor muscle which have short sarcomere length (2-3 pm) and produce twitches which are triggered by overshooting electrogenic responses (10). There are five excitor motoneurons and one inhibitor motoneuron that innervate the superficial flexor muscle. Each axon innervates 40% or more of the muscle fibers, and each muscle fiber receives innervation from at least three axons. In a previous paper (14) it was shown that the probability that a given axon innervates a given muscle fiber was a simple function of the position of the fiber in the muscle sheet. The small excitors decreased their innervation monotonically from medial to lateral, while the large excitors increased their innervation in the lateral direction. Although they are all in the slow range, we found that the different fibers of the slow flexor show a range in size, input resistance, membrane time constant, and resting potential. The five excitor axons innervating the muscle also differ in their properties. The axons are labeled by their size, axon I being the smallest and 6 the largest. Axon 2 has the highest rate of tonic activity (17/s) but produces the smallest jp’s. Axon 6 has the lowest rate of tonic activity (
in U.S.A.
Synaptic Connectivity in a Crayfish Neuromuscular System. II. Nerve-Muscle Matching and Nerve Branching Patterns SAMUEL Department
SUMMARY
J. VELEZ
AND
of Biology,
AND
ROBERT J. WYMAN Yale University,
New Haven,
CONCLUSIONS
I. In the crayfish slowflexor muscle,the input resistance,time constant, resting potential, and size of the muscle fibers change continuously with position from one edgeof the musclesheet to the other. These properties are possibly indications of the relative “slowness” or “fastness” of the musclefibers. 2. The most tonically firing axon (axon 2) innervates preferentially the medial part of the musclewith the “slower” fibers. Its innervation decreasescontinuously in the lateral direction. The fibers innervated by axon 2 do not show a marked position dependence of the measured characteristics. The most phasic axon (axon 6) with the largest (facilitated) junctional potentials (jp’s) innervates in the oppositedirection, innervating mostly “faster” fibers. The fibers innervated by axon 6 do not show a marked position dependenceof their measuredcharacteristics. 3. Most fibers were either innervated by 2 and not by 6, or were innervated by 6 but not by 2. The percentage of fibers belonging to the two groups varies continuously across the muscle, explaining the continuous change in musclefiber characteristic with position. 4. Axons 2 and 6 do not selectively avoid innervating the samefiber. The probability of innervation by both axons in a given region was the product of the probability of innervation by each axon alone for that region. Fibers innervated by both axons had intermediatephysiological characteristics. 5. We proposethat the position of the muscle fiber has no influence, per se, on its differentiation. The mosttonic and most phasicaxons have a trophic or activity-dependent effect, which is responsiblefor the varying musclefiber characteristics. The gradation in muscle fiber properties, then, is due to the gradation of innervation. Received for publication April 2, 1976.
Connecticut
06520
6. Scanning electron micrographswere used to study the branching pattern of the nerve into the muscle. In general, the nerve and its branches run in a medial to lateral direction, but branchescome off at any angle to the main nerve. Branch points appearrandomly scattered over the musclesheetexcept for one prominent backward branch, which always occurs near the middle of the muscle. Comparing right and left sidesof the same animal, there are differences both in the number and location of branches.Comparisonsof the samesidein different animals show roughly comparable dissimilarities. The growth path of the nerve, especially its major backward branch, cannot be explained by a simple growth up or down a gradient. INTRODUCTION
In many animals,vertebrate and invertebrate, there is a “match” between the physiological properties of the muscle fibers and those of the motoneurons which innervate them. This is well documented in mammals, where fast and slow muscle fibers have their corresponding innervation from larger and smalleraxons, respectively (8). In crustaceansthere is also a similar type of matching. Animals have separate phasic and tonic muscles(1). The phasicmuscleshave short sarcomere, rapidly contracting muscle fibers which are driven by phasically firing axons. The tonic muscleshave long sarcomere,slowly contracting fibers driven by tonically firing axons (3). Mixed musclesalsooccur with both types of musclefibers. Somedetailed studies have been made on these mixed musclesand, indeed, in the case where only two axons innervate the muscle fibers, the phasic axon innervates most heavily the short sarcomerefibers of the muscle, while the more tonic axon innervates most heavily the longer sarcomere,slowerfibers(1,2). The superficial flexor muscle of the crayfish 85
Downloaded from www.physiology.org/journal/jn by ${individualUser.givenNames} ${individualUser.surname} (129.059.095.115) on January 13, 2019
86
S. J. VGLEZ
AND
abdomen is a planar sheet of about 40 fibers. The muscle fibers are all of a generally slow type: they have long sarcomere lengths averaging lo- 12 pm and generally exhibit only graded tension changes achieved through summation or facilitation of excitatory junctional potentials (jp’s) (11). This contrasts to the fibers of the synergistic deep flexor muscle which have short sarcomere length (2-3 pm) and produce twitches which are triggered by overshooting electrogenic responses (10). There are five excitor motoneurons and one inhibitor motoneuron that innervate the superficial flexor muscle. Each axon innervates 40% or more of the muscle fibers, and each muscle fiber receives innervation from at least three axons. In a previous paper (14) it was shown that the probability that a given axon innervates a given muscle fiber was a simple function of the position of the fiber in the muscle sheet. The small excitors decreased their innervation monotonically from medial to lateral, while the large excitors increased their innervation in the lateral direction. Although they are all in the slow range, we found that the different fibers of the slow flexor show a range in size, input resistance, membrane time constant, and resting potential. The five excitor axons innervating the muscle also differ in their properties. The axons are labeled by their size, axon I being the smallest and 6 the largest. Axon 2 has the highest rate of tonic activity (17/s) but produces the smallest jp’s. Axon 6 has the lowest rate of tonic activity (
