Where did the motor function of the cerebellum come from?
© Coco and Perciavalle. 2015
Received: 22 June 2015
Accepted: 4 August 2015
Published: 14 August 2015
Until the end of 18th century, the role of the cerebellum remained obscure. The turning point occurred when Luigi Galvani showed that muscle contraction is due to electricity and Alessandro Volta produced the battery, an apparatus based on the pairing of silver and zinc plates separated by brine soaked paper disks, capable to generate electricity. Luigi Rolando, at beginning of 19th century, was impressed by these two observations. He thought that, since the brain generates the movement, it must contain a device generating electricity. As a battery, it should be formed by overlapping disks and the cerebellum for Rolando seemed to be the right structure for such a characteristic laminar organization. He argued that, if the cerebellum is the battery that produces electricity for muscle activity, its removal would produce paralysis. Consequently, Rolando removed the cerebellum in a young goat and observed that the animal, before dying, could no longer stand up. He concluded that the cerebellum is a motor structure as it generates the electricity which produces the movement. The conclusions of Rolando were criticized by Marie-Jean-Pierre Flourens who observed that animals undergoing cerebellectomy were still able to move, even if with problems of balance. Flourens concluded that the role of the cerebellum “is to put in order or to coordinate movements wanted by certain parts of the nervous system, excited by others”. It was necessary to wait up to 1891 when Luigi Luciani, observing a dog survived the cerebellectomy, described a triad of symptoms (asthenia, atony and astasis), unquestionably of cerebellar origin.
KeywordsCerebellum Motor control History
Who was the first to think that the cerebellum could play a motor role? In the Middle Ages, both in Europe and in the Islamic world, scholars believed that outer information from the external senses (touch, taste, smell, hearing and sight) was transferred to the brain to be combined into a unified perception, using a faculty called common sense or inner sense (for review, see Manzoni ).
This inner sense were believed to be housed not in the nervous tissue but in the ventricles of the brain (ventricular theory). It was believed that cerebral ventricles contained the psychic pneuma or vital spirit or animal spirit, a sort of special and light substance endowed with the power to perform sensory, motor and mental activities. The most widely accepted version of this theory was that the synthesized information from the all five senses was located in the front ventricle. Between the front ventricle and the middle ventricle was a storage space for representing previously perceived objects; the space was called the faculty of imagination or representation. The middle ventricle was believed to be involved in cognition and cognitions were thought to be transferred to the rear ventricle, under the cerebellum, for storage with the faculty of memory .
The ventricular theory was challenged from the early 16th century by several European scientists, although some remnants of this theory survived in medicine until the 18th century. In fact, up to the end of that century, the role of the brain structures within the posterior cranial fossa, cerebellum included, remained obscure.
Still in the early 1800s, Franz Joseph Gall (1758–1828), the creator of phrenology, argued that cerebellum is the area of self-preservation of the species .
The turning point occurred thanks to two Italian scientists, Luigi Galvani and Alessandro Volta.
Galvani came to the conclusion that some kind of electricity, which he called animal electricity, was generated in the tissue of the frog and, flowing through the metal rod, activated the frog’s muscles. He thought of animal electricity as a fluid secreted by the brain, and proposed that flow of this fluid through the nerves activated the muscles. He grew convinced that the vital spirit was animal electricity flowing through the nerves and announced this to the Bologna Academy of Science in 1791 .
Alessandro Volta (1745–1827) was professor of experimental physics at the University of Pavia, from 1779 for almost 40 years. In 1792, Volta came to know of Galvani’s experiments on animal electricity. He initiated to repeat the experiments and at first his results agreed with those of Galvani. However, analyzing more closely the experimental conditions, Volta gradually became convinced that the contractions of the frog’s muscles were not due to the presence of electricity generated in the animal, but to some external electricity caused by the contact of the two metals. He concluded that different kinds of metals had electro-motive power at the point where they are in contact with the frog. He summarized his ideas with the expression: “It’s the difference in metals that does it”.
A new hypothesis
Rolando was impressed by the two main observations of Galvani and Volta: muscle contraction is due to electricity and to generate electricity is necessary a battery. His reflection was the following: since the brain generates the movement, it must contain a device generating electricity. In his book published in 1809 , he writes “se i fenomeni della locomozione sono l’effetto di un particolare meccanismo, questo non altrove che nell’encefalo andava ricercato”. (if the phenomena of locomotion are the effect of a particular mechanism, this not elsewhere than in the encephalon had to be researched)
For Rolando this part of the brain, as a battery, should be formed by overlapping disks and the cerebellum seemed to be the right structure given its characteristic overlapping laminae, forming the so-called arbor vitae. Probably the term was coined by the Danish anatomist Jacob B. Winsløw (1669 –1760) for the similarity of cerebellar folia with the profile of leaves of the North American tree Thuja occidentalis or Eastern Arborvitae, introduced in France in 1534 by French explorers. It seems that the tree was named “l’arbre de vie” by the King Francis I  for analogy with the use of this expression in the Book of Proverbs, where the tree of life is associated with wisdom.
Rolando writes “se dunque l’organo elettrico torpedinale e quelli del Siluro e del Ginnoto, fatti di sostanza albumino-gelatinoso-cartilaginea e simili attissimi sono a preparare, ed a sviluppare una quantità grandissima di fluido elettrico sufficiente per dare grandissime scosse, perché non potrà separarsi un principio consimile, quale si è il nerveo fluido dalle numerose lamine di sostanza midollare, giallognola, e cinerea del cervelletto? Quale maggiore evidenza potrassi desiderare per stabilire, che il cervelletto è un organo, la cui struttura è affatto consimile a quella dell’apparecchio del Volta?” (if the electric organ of torpedo and those of wels catfish and electric eel, made of albuminous-gelatinous-cartilaginous substance, are perfectly suited to prepare and develop a large amount of electric fluid enough to give huge shocks, why a similar principle should not take place in form of nervous fluid from several sheets of yellowish and cinereous substance of the cerebellum? What greater evidence can be desired to establish that the cerebellum is an organ whose structure is absolutely similar to that of the Volta’s device?).
Rolando concluded that, if the cerebellum is the battery that generates electricity for muscle activity, its removal would produce paralysis. He writes “Qual maggior prova per dimostrare, che dal suddetto viscere si separa un fluido analogo a quello, che dallo strumento citato si sviluppa? Qual più retta conseguenza, se esportato guasto o distrutto il cervelletto cessa ogni influsso del fluido nerveo nei muscoli destinati alla locomozione?” (What most evidence to prove that the said organ generates a fluid similar to that which develops from the mentioned device? What most direct consequence if removed, destroyed or spoiled the cerebellum ceases any influence of the nervous fluid on the muscles for locomotion?).
Rolando, consequently, removed the cerebellum in a young goat and observed that the animal could no longer stand up “non altrimenti che se fosse paralitico” (not otherwise than if it was paralyzed). The animal survived for 24 h and died probably for postoperative sepsis.
Rolando concluded that the cerebellum is a motor structure as it generates the electricity which produces the movement.
Since also its animals died shortly after the operation, Flourens hoped that the improvement of the surgery would allow to have animals surviving the cerebellectomy, to clearly distinguish the deficits due to the removal of cerebellum from those related to postoperative complications.
The first systematic description of the symptoms of cerebellar lesions in man was carried out by the British neurologist Gordon Morgan Holmes (1876 –1965). During World War I he was neurologist with the British Expeditionary Forces and working in a field hospital he had the opportunity to investigate the effects of traumatic lesions involving the cerebellum. In 1922 Holmes’ observations on patients with cerebellar wounds as well as tumors were published in his Croonian Lectures to the Royal College of Physicians .
The general conclusion reached before World War II was that the main role of the cerebellum is to detail the different aspects of a movement, not to initiate movements or to decide which movements to execute. After the war, there was a significant increase in knowledge of circuitry and electrophysiology of the cerebellum, summarized in 1967 in a book, The Cerebellum as a Neuronal Machine , written by the Nobel laureate John C. Eccles (1903–1997), Japanese neuroscientist Masao Ito, and Hungarian anatomist János Szentágothai (1912–1994), followed in 1974 by a review, Cerebrocerebellar communication systems , written by two neurophysiologists, the American Gary I. Allen and the Japanese Nakaakira Tsukahara (1933–1985).
In the same years it was suggested that the cerebellum is involved in motor learning. Most theories that attempt to explain the role of cerebellar circuits in motor learning are derived from the ideas of British neuroscientist and psychologist David C. Marr (1945–1980) and of American engineer James S. Albus (1935–2011). Both attributed an important role to climbing fiber activity capable to cause synchronously activated parallel fiber inputs, to be strengthened for Marr  and to be weakened for Albus . In the 1980s, the discovery in the cerebellum of Long Term Depression (LTD) was considered as a form of synaptic plasticity involved in motor learning. LTD occurs when impulses of a set of granule cells and one climbing fiber reach the same Purkinje cell synchronously and repeatedly; synaptic transmission from the granule cells to the Purkinje cell is then persistently depressed . Although LTD is now well characterized, its contribution to motor learning remain controversial .
Major contributions to the current knowledge of the cerebellum
The cerebellum is the battery that produces the electricity necessary for generating muscular contraction
The role of the cerebellum is not that of generating the movement but to regulate it
Description, in a dog survived the cerebellectomy, of a triad of symptoms (asthenia, atony and astasis) unquestionably of cerebellar origin
Santiago Ramón y Cajal
Publication of the first modern textbook of neuroanatomy with a clear description of the cerebellar cortex.
Gordon Morgan Holmes
Systematic description of the symptoms of cerebellar lesions in man
John C. Eccles, Masao Ito, and János Szentágothai
Book: The Cerebellum as a Neuronal Machine
David C. Marr
Hypothesis about cerebellum and motor learning: A theory of cerebellar cortex
James S. Albus
Hypothesis about cerebellum and motor learning: A theory of cerebellar function
Gary I. Allen and Nakaakira Tsukahara
Review: Cerebrocerebellar communication systems
Masao Ito and Masanobu Kano
Description in the cerebellum of the Long Term Depression
Jeremy D. Schmahmann
Description of the Cerebellar Cognitive Affective Syndrome
Luigi Rolando devoted his life to the study of the brain. Despite his outlandish theory on the cerebellum, he provided a major contribution to the advancement of neurosciences and many neural entities are named after him: the substantia gelatinosa of Rolando in the spinal cord, the fissure of Rolando or central sulcus, the Rolandic operculum or post-central operculum, the Rolandic artery or central sulcal artery, the Rolandic vein i.e., the vein posterior to Trolard’s vein draining the parietal lobe, the pre-Rolandic artery or precentral sulcal artery, and the Rolandic epilepsy or benign childhood epilepsy with centrotemporal spikes (BCECTS), the most common epilepsy syndrome in childhood.
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