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European Journal of Applied Sciences – Vol. 12, No. 2

Publication Date: April 25, 2024

DOI:10.14738/aivp.122.16871

Swatland, H. J. (2024). A Review of Motor Innervation in Growing Meat Animals. European Journal of Applied Sciences, Vol - 12(2).

347-356.

Services for Science and Education – United Kingdom

A Review of Motor Innervation in Growing Meat Animals

Howard J. Swatland

Department of Animal Biosciences,

University of Guelph, Guelph, Ontario, Canada

ABSTRACT

Meat animals have been bred to have enormous muscles. The genes regulating

myogenesis and muscle growth are now becoming known. How does the motor

innervation interact with massive increases in myofibre diameters and numbers?

Stress-susceptible pigs have myofibres with a ryanodine mutation in their calcium ion

release channels. This leads to excessive muscle activation and the hypertrophy of

fast-contracting myofibres. These myofibres develop large neuromuscular junctions,

often with extra axonal sprouts and double motor end plates. Mutations in the

myostatin gene cause myofibre hyperplasia in double muscled cattle. Terminal axons

have increased branching to innervate the extra myofibres. The number of

neuromuscular spindles to give feedback to the cerebellum is increased and

spindles have more intrafusal myofibres regulating feedback. Is the motor

innervation merely responding to the increased muscle mass, or is this an

interactive system?

INTRODUCTION

In the 1970s, genomics was in its infancy, few genes were known except those in experimental

animals. But at this time, a variety of problems and possibilities in meat production were being

urgently investigated. On one hand, stress-susceptible pigs notorious for producing pale, soft,

exudative pork were threatening the profitability of fast-growing breeds. On the other hand,

double-muscled cattle offered great possibilities if their reproductive problems could be

overcome. Biochemists and histologists were soon at work and discovered many things. But

between genotypes and phenotypes there are many epigenetic mechanisms still worthy of

continued investigation. This historical review examines the role of the nervous system in

growing meat animals, historical because there is very little new to review.

Meat animals provide a unique situation for investigating neuromuscular interactions. For

countless generations of meat animals there has been a relentless increase in muscle mass and

growth rates. Muscle mass may be evaluated in terms of myofibre hypertrophy and hyperplasia,

but what about the motor innervation? As the genes for myogenesis and muscle growth become

progressively better known, it might be time to reconsider how they interact with trophic

factors from the motor innervation.

TROPHIC EFFECTS

Pioneer physiologists were aware that denervated organs usually undergo a series of

degenerative changes culminating in a severe loss of function [1]. This phenomenon was

particularly obvious in skeletal muscles. Trophic neural functions regained importance with

the crossed-reinnervation experiments of Buller, Eccles and Eccles [2]. The basis of a crossed-

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European Journal of Applied Sciences (EJAS) Vol. 12, Issue 2, April-2024

reinnervation experiment is to transect two nearby nerves that innervate separate muscles

with different contraction speeds, and then to re-unite the proximal end of one nerve with the

distal end of the other nerve and vice versa. When successful, this experimental manipulation

results in both muscles becoming reinnervated — but by crossed nerves. Contraction speeds

change according to their new innervation.

Is the neural effect nerve on muscle caused by the activity patterns imposed by the nerve on

the muscle or to the passage of some type of trophic substance to the muscle? The activity

pattern hypothesis is that myofibres that are frequently stimulated to contract tend to become

specialized for tonic activity [3]. Tonic activity is indicated by slow ATPase (myofibrillar

adenosine triphosphatase) and a slow contraction speed coupled with a strong capacity for

aerobic metabolism. Conversely, myofibres that are used infrequently but with an intensity that

can only be supported by anaerobic glycolysis tend to develop a fast ATPase and contraction

speed coupled with a reliance on anaerobic metabolism. There is evidence that extrinsically

programmed activity may regulate the metabolic specializations of myofibres together with a

trophic effect [4].

There was a surge of interest in the motor innervation controlling muscle metabolism in the

1940's [5]. When constricting rings were clamped around distal axons it was discovered that

the diameter of the restriction limited the diameter of the regenerating axon once it had grown

through the ring on its way to the periphery. Upstream of the restriction, towards the motor

neuron cell body, the regenerating axon was swollen. When restrictions were removed, the

damming of the axoplasm was relieved and the diameter of the distal part of the axon was

enlarged. Three essential features of the system thus became apparent: (1) that axoplasm was

synthesized in the motor neuron cell body around the nucleus; (2) that the peripheral flow of

axoplasm was matched to the axonal diameter and; (3) that there was a continuous catabolism

of axoplasm all the way down the axon so that the peripheral endings of normal axons did not

explode with the continuous influx of axoplasm.

INTRAMUSCULAR INNERVATION

When a motor axon enters a muscle, it branches to innervate all the scattered myofibres of its

motor unit and the pattern of intramuscular nerve branching in pennate muscles may follow the

regional histochemical differentiation of myofibres [6]. The situation in meat animals is very

complex because of their enormous muscles and it is unwise to assume that the zone of myofibre

innervation is in an equatorial plane. Even in the small peroneus longus muscle of the pig which

has short fasciculi with all myofibres running from origin to insertion there are two innervation

zones [7].

The terminal axon is the final axonal branch that innervates a muscle. The functional terminal

innervation ratio (FTIR) is the mean number of myofibres innervated by the axonal branches

radiating from an intramuscular nerve. The absolute terminal innervation ratio (ATIR) gives the

mean number of motor end plates innervated by the axonal branches radiating from an

intramuscular nerve. There is a considerable subjective element in deciding how far back into the

intramuscular nerve that branch points are to be recorded but, if standardized, the distal sample

of the total degree of axonal branching is a useful measure of changes in the total amount of axonal

branching.

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Swatland, H. J. (2024). A Review of Motor Innervation in Growing Meat Animals. European Journal of Applied Sciences, Vol - 12(2). 347-356.

URL: http://dx.doi.org/10.14738/aivp.122.16871

In muscles from healthy pigs, the FTIR ranges from approximately 1.00 to 1.04. The ATIR ranges

from approximately 1.01 to 1.13 because some myofibres have double motor end plates [7]. Motor

end plates might have a limited life span, and double motor end plates may be a phase in the

physiological replacement of motor end plates [8]. But there are many other possibilities and, as

yet, no definitive proofs [9]. Looking for ways in which motor innervation might have adapted to

greatly increased muscle mass, double motor endplates on large diameter myofibres are a

possibility.

MOTOR UNITS

Each motor neuron innervates a number of myofibres in the same muscle and the group of

myofibres innervated by a single neuron is called a motor unit. The myofibres of each motor unit

exhibit similar metabolic features [10]. The myofibres of a motor unit are scattered through the

muscle, but they tend to form clusters rather than following a truly random distribution pattern

[11]. Further mechanical integration of contraction may be caused by the longitudinal dispersion

of motor units along the muscle, where they often follow the fascicular or connective tissue

architecture the muscle [12]. When muscle contraction is initiated by the nervous system, motor

units are generally recruited in a fixed order related to the size of the perikaryon. Neurons with a

smaller perikaryon are more readily activated than larger neurons.

In short muscles, individual myofibres may extend without interruption from one end of a

fasciculus to the other. But, in muscles with long fasciculi, many myofibres have tapered endings

that do not reach to the end of the fasciculus. These are called intrafascicularly terminating

myofibres. Tapered endings are anchored in the endomysial connective tissue around an adjacent

normal diameter myofibre. Contraction of an intrafascicularly terminating myofibre may stretch

the myofibre on which it is anchored. Not only might the series elasticity of the passive myofibre

change the result of a contraction by an intrafascicularly terminating myofibre, but the response

of the stretched myofibre will also be changed if, in turn, it is stimulated to contract. Thus, the

distribution of intrafascicularly terminating myofibres may enhance the neural mechanisms

(firing rate and motor unit recruitment patterns) that are responsible for the smooth production

of muscle force. In attempting to understand muscle growth in meat animals, the major problem

created by intrafascicularly terminating myofibres is that their presence makes it impossible to

reduce muscle mass to a question of myofibre diameters and number of myofibres. Muscle mass

may be increased by intrafascicularly terminating myofibres increasing in length.

Most myofibres have a motor end plate about half way along their length. Neuromuscular

junctions are established very early in development, and a considerable length of new material is

subsequently added to each end of the myofibre so that the motor end plate remains in the middle.

Many muscles have relays of fasciculi, each with a zone of motor end plates and myofibres may

extend through two innervation zones with an end plate in each [13]. In this case, however, it is

difficult to prove that both end plates do not originate from a single axon that branched before

reaching the muscle. The consensus at the present time is that multineuronal innervation of

mammalian myofibres may occur in immature muscles that are still establishing appropriate

neuromuscular connections, but this only persists for a short while after birth and then is lost (Fig.

1). A developing neuromuscular spindle takes control of myofibres when they are at the primary

stage of development being derived from myoblasts fusing to make primary myotubes with axial