Yakovlev - 1989 Obituary

J. Neurolinguistics, Volume 4, Number 2, pp. 273-292, 1989. 091 l-6044/89 8.3.00 + .OO Printed in Great Britain Pergamon Press plc

Paul Ivan Yakovlev and His Teachings on Cerebral Maturation and Asymmetries1

Andrk Roth Lecours2

Centre de recherche du Centre hospitalier C&e-des-Neiges,

Montr6alJ

ABSTRACT Indications about the life and scientific career of Paul Ivan Yakovlev are presented in

the first part of this paper. This is followed, in the second part, by a summary of his conceptions on the ontogenesis of the human telencephalon: his ideas concerning

embryologically constrained distinctions (a) between telencephalon impar (rhinic). semipar (limbic), and totopar (supralimbic), as well as (b) between endokinetic (“cell- bound”), ereismokinetic (“body-bound”), and telekinetic (“object-bound”) motilities are then discussed in relation to his teachings on primary (“formal”) as opposed to secondary (“positional”) symmetry. The third and fourth parts are devoted to Yakov-

lev’s ideas concerned the asymmetries of the human brain; the research that he led with Pasko Rakic on the asymmetry of the pyramidal decussation and tracts is then summarized. The fifth and last part of the paper is based on an operational definition of the Yakovlevian notion ofmyelinogenetic cycle; a parallel is then drawn - in relation to differences in the moments at which auditory and visual information enter into play as parameters of functional ontogenesis as well as to differences in the functional deter- minisms of these two basic types of information - between the long biphasic cycle of the acoustic pathway as opposed to the short monophasic cycle of the optic pathway.

PAUL IVAN YAKOVLEV (1894-1983)4

The town of Turetz is located at 55,22’ North and 29,15” East of the Greenwich meridian, “at the median point of a line separating the Orient from the OccidenP. This is where Paul Ivan Yakovlev was born in December of 1894, the 15th according to the Julian and the 28th according to the Gregorian calendar. His

274 Journal of Neurolinguistics, Volume 4, Number 2 (1989)

aristocratic mother spoke French with members of her family (she considered

Russian to be a language one should speak with servants or at the market, but not

with one’s kins); his father was a retired imperial army officer who enjoyed taking

his son for long walks in the snow. An orphan at the age of nine, Paul Ivan was sent

to live in Wilno, with his widowed maternal aunt, who was the mother of three

daughters and the director of “a private gymnasium for girls”.

As an adolescent, Paul Yakovlev decided that he would become a philologist,

perhaps an historian, or else a painter, or perhaps a sculptor. Then time passed and

he changed his mind: he thought very highly of his father’s father, a military

surgeon, and began to consider medicine as a potentially fulfilling career. An artist

“has to be a genius or else one isn’t worth while , . . but in medicine allyou have to do is read books, remember it all and you know all the answers.” In 1914, he

obtained his baccalaureate from the Classical Gymnasium of Wilno. He was 21

years old, in 1915, when he was awarded a Sir Jacob Wylie Fellowshipband entered

the Saint Petersburg Imperial Academy of Military Medicine, with the intention

of becoming a psychiatrist, “a doctor who would manipulate the soul, make it

happier, healthier.”

During the period when Saint Petersburg was becoming Petrograd before it

became Leningrad, Paul Ivan Yakovlev grew less and less interested in unleashing

“the secrets of the psyche” and more and more in “what was called in those days

organic psychiatry”, in which “everything had to have a mechanical explanation”.

He studied histology with Alexandre Maximov, who was “scholarly, H+th diligence

qf’presentation”, organic chemistry with Alexandre Borodine, who kept his grand

piano in his laboratory at the Academy, and physiology with Vladimir Mikhailo-

vitch Bekhterev, the founder of Russian neurology, who remained active although

he had recently retired, and later with Ivan Petrovitch Pavlov, a most impressive

man whose lectures on conditional reflexes were indeed fascinating, and whose

‘extreme!)’ antipsJ!chologj” orientation was a topic of passionate discussions

among the students of the Academy. This was a troubled period, but young

Yakovlev had great masters and he was soon convinced that his own life could only

be devoted to the acquisition of scientific knowledge.

During the summer vacations of 1916 and 19 17, Paul Ivan Yakovlev served as a

stretcher-bearer in the Imperial Army. Then came the October Revolution. There-

after, the Academy was no longer “Imperial” though it was still a medical school,

and a good one. In 1919, Petrograd fell prey to famine, typhus, Spanish influenza

and civil war: the population was terrorized and confused. At the end of the year,

Trotsky’s Red Army needed physicians: the students of the Academy therefore

received their diplomas six months ahead of time, on 25th December. Paul

Yakovlev was genuinely apolitical but he could not conceive how Russia might, in

any future that he could now foresee, provide him with the opportunity to carry on

Paul Ivan Yakovlev and his Teachings 215

with his scientific education. Moved by a powerful feeling of “instinctive biological

survival” and after consulting with Maximov, he took the decision to leave his

country. On the morning of 27th December, he and a Polish colleague, Trachinski,

pretending that they had been charged with a public health mission, boarded a train

heading for the Finnish border where local Finn and White Russian as well as

English, American and German troups were closely watching the movements of the

Trotskyst army. In order to avoid showing their“manufacrured.. . cerrificate”and

answering the questions of the “red arm,’ inspector, the police, the inspector

controlling the passports," the two companions “navigated” from one wagon to the

next till they found themselves on the crowded rear platform of the train. Alongside

the railroad tracks, there were snowy woods and, beyond the woods, the Gulf of

Finland, frozen solid. In spite of bitter cold winds, Paul Yakovlev and his friend

persuaded one another that the Gulf constituted the shortest and safest route out of

Russia. Twenty kilometers or so before the border, in the middle of the night,

dressed with several layers of clothes, they slipped off the slow moving train and

they started walking in the snowstorm. Beside their certificates and diplomas, they

carried black bread, bacon, a revolver, a compass, 800 Imperial Rubles and white

blankets. The latter were used whenever the generators of searchlights were heard

and beams rippled too close (one then flopped down, covered oneself, and hoped

one had become invisible). At one point, Trachinski extirpated a bottle from his

bag: it contained a pinkish mixture of laboratory alcohol and something else

“(cocaine?)“: Paul Ivan’s companion had stolen the ingredients at the Academy on

Christmas Eve and the concoction now turned out to be of the greatest help. When

the sun rose, on 28th December, the day of Paul Yakovlev’s 25th Gregorian

anniversary, the two reached the shore and sought safety inside empty barrels near

a deserted cement factory. A dog passed by, sniffed at the terrorized fugitives, and

wandered on: a stray dog that had long learned that minding one’s own business

was now a behaviour making one’s survival more likely. With night coming,

Yakovlev and Trachinski resumed their outing toward destiny. At the dawn of 29th

December, as they emerged from the snowy bushes bordering on the Gulf, the pair

were arrested by Finnish guards. Unbelievably, one of them recognized Paul

Yakovlev from a previous visit to Petrograd. This made things easier but the

“comp>res” were nonetheless sent to Coventry: the Finns accepted refugees from

Russia only when sure that they were not attacked by typhus or some other dreadful

disease. The two survived quarantine, shook hands, and parted forever: Trachinski

was heading for Siam (where he intended to study butterflies).

Paul Ivan Yakovlev spent a few months in Finland, attending to odd jobs in

Helsingfors’ at one time and in AaboX at another time. He then decided that the day

had come for him to find a place where he could resume his scientific quest: given

the interest that he had in psychic disturbances resulting from brain damage, and


also given the advice of his professors in Petrograd, his target was the private clinic

which Hermann Oppenheim had opened in 1890, after having been denied

Westphal’s succession by the Prussian Secretary of Education, and which had

progressively outclassed the Charite as the international center of clinical neuro-

logy in Berlin (Weil 1970). The Russian in exile therefore presented himself at the

German embassy with his Academy diploma and a few letters of recommendation

written by his Russian professors: but Oppenheim had died earlier in 1919, before

Yakovlev’s mentors dated, wrote and signed their lettersand the recommendee was

now suspected of counterfeiting. As these events required reflexion and reorien-

tation, Paul Yakovlev decided to stay in Helsingfors a little longer. Until March

1920, he worked in the harbour where his job was to inspect a cargo of Swedish

matches “(“Vu/can”)” that had been damaged by sea water: for a few months, he

hand-picked boxes - “dry matches on onesideand M-et ones on the other”- while

pondering various scenarios: Germany being excluded, where to go next? France

and the Salpetriere: after all. he was quite fluent in French and he had read

everything that Charcot and his disciples and successors had written.

In April, Paul Ivan Yakovlev boarded a ship to England. In London, as in the

other great capitals of Western Europe, it was generally believed that Bolchevism

would not survive and the Russian embassy had remained faithful to the Tzar:

there, refugees would easily trade Rubles for Sterling. Yakovlev could survive and,

after having by chance discovered the existence and seat of the British-Russian

Brotherhood Society, he was even able to earn an extra hundred Pounds writing

reports on the state of public health in Russia since the Fall of 1917.

The fourth of October, 1920, was the day of the first commercial flight between

London and Paris: Paul Yakovlev did not have enough money to buy a ticket and

he experienced considerable frustration, but, the very same day, he procured a

place on the boat-train that travelled from London to Paris via Doverand Bologne.

In the Latin Quarter of Paris, Paul Ivan Yakovlev rented a room in Madame

Bourdon’s boarding house, near the Pantheon. Of Madame Bourdon, he was later

to say, with obvious fondness and gratitude, that she was very strict as to monthly

payments but acted in a motherly manner with the “petits metPques” from Haiti,

Paraguay and Mexico who were then her guests, including this “petit metPque

russe” who, whatever the hour of day or night, paced back and forth his limited

“private space above the entresol dining room (‘Monsieur Yakovlev, vous Btes un

maniaque!‘)“. A few days after his arrival in Paris, Yakovlev rang at Charles

Richet’sg door and told him that he came on behalf of a Professor Daniel Gardner,

from Cambridge. He explained that he had met and befriended Gardner in London

and he presented Richet with a recently written recommendation. Richet sym-

pathetically introduced the young Russian physician to “a dearest ,fiiend”,

Madame Abrikossov, one of the last of Charcot’s students, who had retained


friendly relationships with the Salp&ri&re. Soon thereafter, Paul Yakovlev became

a “stagiuire Ptrunger” at the Clinique des maladies du systeme nerveux where, after

Fulgence Raymond and Joseph Jules Dejerine, Pierre Marie had finally fulfilled his

desire to take over Jean-Martin Charcot’s chair.

At the Faculty, Yakovlev’s medical studies in Russia were recognized but, in view

of local requirements, he would have to pursue further internship in obstetrics,

paediatrics, gynecology and . . . infectious diseases. The candidate happily com-

plied, agreeing that, at least for three out of four, these requirements appeared to be

reasonable in view of the fact that he had graduated from a military institution.

When Pierre Marie retired and yielded Charcot’s chair to Georges Guillain,

Yakovlev went to work at the Pitit, next door to the Salpetritre, with Joseph

Francois Felix Babinski: he had found the man who would guide him in his

doctoral research and dissertation, and whom he would forever consider as his

Mentor. It was at the Pitie that Paul Yakovlev began to develop an interest for the

effects of sensory disturbances on motor behaviour; he became involved in dis-

cussions concerning cerebral lesions leading to paraplegia in flexion, a problem

which one of his colleagues, Thtophile Alajouanine’“, was studying in the context

of his doctoral research.

Informed that his new student was somewhat needy, Babinski found a job for

him: Yakovlev would work as an “inrerne de nuit” in a fashionable Neuilly

Sanatorium, where many “parients” were politicians in need of temporary invisi-

bility or rich American addicts taking a detoxication cure. Accommodations were

exceptionally good and emergencies infrequent: the place was excellent for one

who had an appointment in a large university hospital (the Pitie, then Sainte-Anne)

and had to spend after-duty hours studying and writing a doctoral dissertation.

Entitled “Associations pithiato-organiques”, i.e. motivated by one of Babinski’s

major preoccupations in those days, the dissertation was published at the end of

1924 - one year after Alajouanine’s - by the Presses Universitaires de France.

Paul Yakovlev defended it publicly two days after the Epiphany of 1925 and his

board of examiners was comprised of Professors Achard, Sichard and Balthazar! 11

At this point, Paul Ivan Yakovlev considered the prospect of pursuing his career

in France. As a matter of fact, he enjoyed the idea but this scenario was excluded

since it would mean having to take French citizenship, which in turn would imply waiting several years and regressing for a time to high-school level training and

examinations. Other scenarios were also rejected: he remembered the ambiguous

feelings he had experienced during a trip to Berlin, in 1923, and decided that his

professional perspectives were no better in Germany than in France; and he

definitely renounced the idea of returning to Russia where “dust had not settled

afier all”. On the other hand, he was corresponding with Alexandre Maximov, who

had migrated to the United States in 1921 and was now teaching at the University of


Chicago: Maximov now insisted that the land of opportunity for an ambitious

scientist was no longer Western Europe but the USA. Moreover, Paul Yakovlev

had had, as a patient in Neuilly, an American physician from Providence, Rhode

Island: this colleague had introduced him to an “attache” of the American embassy

in Paris; the “attach&” had an influential uncle who was an archbishop somewhere

in Ohio; consequently, soon after defending his dissertation, Yakovlev was offered

an “extra quota American passport” on the basis of his “exceptionalproj&sional

quallyications”.12 He accepted without hesitation, packed his books, his brand new

diploma from the Universite de Paris and a few other things and, on 15th March

1925, he boarded a ship leaving Le Havre for New York. In April, he became the

“assistant” of a neurologist who was practicing in Providence; the newspapers told

of (nothing less than) an “eminent collaborator Oj’Babinski” who had travelled all

the way from Paris to Providence in order to complete his neurological training

with a famous local practitioner. But the eminent collaborator found it difficult to

live on 20 dollars a month and, above all, his idea of being a neuroscientist was

indissociable from that of obtaining an appointment in a university of renown:

Boston was the aim.

At the Boston City Hospital, Stanley Cobb, William Lennox and Tracy Putnam

had developed a major interest in epilepsy. Cobb and Lennox were preparing a

monograph on the subject and a young enthusiastic competent polyglot neurologist

who could review the foreign literature was a highly desirable collaborator. Paul

Yakovlev’s salary increased from 20 to 150 dollars a month: he served in the

outpatients clinics of the hospital and, as a Harvard Research Fellow in Neurology,

he read and took notes. The review was completed in June, 1926, and, in July, he

began to work in Palmer, Massachusetts, as a neurologist and neuropathologist of

the Monson State Hospital for the Epileptics. He had established good contacts

within the Harvard Neurological Unit at the Boston City where, for several years,

he would spend at least one week every month: he considered himself “the Harvard

liaison man at Monson”. His research career had begun and his first American

paper - “Epilepsy and Parkinsonism” - was soon to be published in the New

England Journal of Medicine.

In the Fall of 193 1, Paul Yakovlev borrowed 1000 dollars and travelled to Paris,

then to Bern where the very first international meeting entirely devoted to

neurology was taking place. This was for him the occasion to meet again with a

man for whom he had the greatest admiration and respect: Ivan Pavlov, who had

serenely begun his ninth decade, had travelled to Switzerland for the occasion.

Harvey Cushing was also there to report on the more than one thousand cases of

brain tumour on which he had operated, and no doubt to insist on the necessity

of surgical treatment for patients with pituitary adenoma (now 78, retired and

living on the C8te d’Azur, Pierre Marie, whose studies of acromegalia have


become classical, although “he has missed the adenoma”, had not made the trip).

After the meeting, Yakovlev took the train to Zurich where he spent seven

months working with Mieczyslaw Minkowski (at Von Monakow’s Hirnanato-

misches lnstitut) and acquired a Masters degree in neuroanatomy. Once in Zurich

and as the result of Minkowski’s intervention, he reclaimed the celloidin embedded

anatomical specimen that he had brought in his luggage but had been forced to

leave at the Swiss border in order to avoid the needle probing procedure of a

zealous customs officer searching for smuggled diamonds. The specimen was the

brain of a two year-old boy whom he had observed at Monson and whose autopsy

he had performed. Remembering the Dejerines’ way of preparing brains in gapless

serial sections, Paul Yakovlev planned to learn the technique in Minkowski’s

laboratory. He travelled back to New England in March, 1932, with heavier

luggage: he brought back the slides of the first specimen of the Yakovlev Collection

(a case of the condition which he would label as “schizencephaly” in a classical

publication yet to come). Later that Spring, Paul Ivan Yakovlev received an

appointment as Assistant in Neurology at Harvard Medical School. He then wed

Mary McQuaid and spent his honeymoon in Montreal, a city he knew quite well as

the result of a few ‘gamboling expeditions during the prohibition years”. Back

home again, he started making plans to build his first giant microtome: modelled

after a smaller one, designed and produced several years earlier by Milton and

Robert GoddardiJ. Yakovlev remained at Monson until 1938, gathering materials

for his Collection’4, researching and publishing on topics such as neurosomatic

deterioration in epilepsy, the anatomoclinical correlations of myoclonus in epi-

lepsy, decerebrate rigidity, congenital ectodermoses, hepato-lenticular degenera-

tion and paradoxical tendon reflexes.

Paul Ivan Yakovlev’s “official baptism in Harvard Neurology” (Livingston

1973) occurred in 1938 when he left Monson for the Fernald State School where, in

194 1, the Assistant in Neurology graduated to Instructor in Neurology. This was

where he remained until 1947, relentlessly pursuing his researches: the giant

microtome was perfected; new specimens were collected and prepared in serial

sections. Topics already approached were further studied and new ones were

tackled: tuberous sclerosis (and “brain stones”), the plantar reflex “as a criterion of

endurance” preceded by “locomotion and the plantar reflex” in mental deficients as

opposed to normals (Yakovlev remembered what he had learnt with his French

Mentor), porencephalies (some of the most spectacular specimens of the Col-

lection), Morquio’s disease, Hallervorden-Spatz’ disease, carbon monoxide

poisoning, hydrocephaly, and so forth. In 1942, his postgraduate seminars in

neurology and psychiatry, of which he later claimed that they were “the beginning

of continued education system in medicine” (Kemper 1984), were published by the

Waltham State Metropolitan Hospital (with the support of the Rockefeller


Foundation). In 1942, with Roy Dennis Halloran, Paul Yakovleveven published a

“Course in Military Neuropsychiatry” and, in 1944, with Harry Solomon, a “Manual” of the same.

Paul lvan Yakovlev thereafter spent four years at the Middletown State Hospital

and at the Yale University Medical School as a Clinical Associate Professor of

Neurology (1947-1951). He developed a training program which became very

popular among Connecticut physicians, including residents and Faculty members.

The first trinity paper - telencephalon impar, semipar, totopar; endokinesis,

ereismokinesis, telokinesis (cf. infra) - was published in 1948; it was followed by

publications on Heller’s syndrome, various types of brain malformations, the

anatomical substratum of seizures, and so forth. The Yale Venture came to an end

due to divergencies with “the local pundits qfpps?,~hoanal_vsis”. “Harvard knows a good man when it sees one, especially a man who has

previously served Harvard and who is ‘farmed out’, so to speak, at another

prestigious school. So Harvard invites Paul to ‘come home”’ (Livingston 1973): in

1951, he was appointed as a Clinical Professor of Neuropathology at Harvard

Medical School. He thereafter went on with his research: the fronto-pontine

bundle, fronto-thalamic projections, paraplegia in flexion (a tip of the hat to

Theophile Alajouanine), meningo-facial angiomatosis, the cytology of the geni-

culate nuclei, the “crowbar skull”, leukodystrophies, the connections of the tem-

poral lobe in man, cerebral calcifications, brain anatomy in mental retardation, the

limbic nuclei of the thalamus and the connections of the limbic cortex, the cingulate

gyrus and its cortico-cortical connections, stereotaxis, localization of thalamic

lesions. handedness (cf. infra), myelinogenesis (cf. infra), Parkinson’s disease,

cerebral infarctions in the human fetus, the decussation of the bulbar pyramids(cf.

infra), the development of the corpus callosum, and so forth: Paul Ivan Yakovlev

was enjoying his Collection. In 195 1, he was elected President of the American

Association of Neuropathologists. In 1954, with Singer, he published anatlas of the

human brain in sagittal sections and, in 1974, with Angevine and Mancall, an atlas

of the human cerebellum.

Between the time of publication of the two atlases, Paul Yakovlev had been

appointed consultant in neuropathology at the Peter Bent Brigham Hospital

(1954) at the Children’s Medical Center (1956) and at the Massachusetts General

Hospital (1961). He had become a Professor Emeritus (1961). the Curator of the

Warren Anatomical Museum (1961); he had travelled the world overrs, and he had

become a living legend (Figure 1). Year after year, he had been the respected

fatherly and inspiring mentor of students and scholars from all over the world - in

Derek Denny-Brown’s words, “he has acted as a catalyst on generations after

generations of neurologists and psychiatrists”; he had taught clinical neurology,

neuropathology, neuroembriology, neuroanatomy; he had explained the import-


ante of seeking relationships between brain maturation and the emergence and

differentiation of behaviours, in humans and in other animals; he had invited

everyone for sharp Cheddar and vodka at 21 Addington Road, Brookline; he had

frightened everyone with his very peculiar manner of driving beat-up cars

through the streets and tunnels of Boston; and he had earned both the indefectible

friendship and the admiration of most. He lost neither when he relocated the

Collection at the Eunice Kennedy Shriver Research Center, in 1969, and, in 1974, at

the Walter Reed Medical Center.

The Yakovlev Collectionrh: more than 1000 whole brains embedded in celloidin

and prepared in gapless serial sections (27 tons of glass; Haleem 1984); brains of

humans. monkeys, dolphins and other animals; normal brains and pathological

Figure 1. Paul Ivan Yakovlev (1 April 1982).


ones; foetal brains, young brains, adult brains, senescent brains. The giant micro- tomes had been put to good use. And, with the Collection, the personal library: some 2000 books and 5000 reprints. Altogether, a material that has proven tremendously useful in the past and should remain available, now that Paul Yakovlev has died, on 16 June 1983, to be used by generations to come.

“Those who knew him will cherish their memories of the kind, sensitive, gentle man who was a trusted and loyal friend, advisor, mentor, confidant, and constant source of inspiration” (Kemper 1984).

TELENCEPHALON IMPAR, SEMIPAR AND TOTOPAR

As mentioned in the biographical notes above, the first specimen of the Yakovlev

Collection, the one that Paul Ivan Yakovlev carried in his luggage during his 193 l-32 European trip, was the brain of a schiiencephalic child. As a matter of fact, it was not so much malformation per se that motivated his curiosity for this and several other gross embryological CNS anomalies (in particular those determined at the time of emergence of the optic vesicles), but rather what could be learned about the normal ontogenesis of cerebral structures and functions through the morphological study of genetic aberrations (Yakovlev 1952). In this respect, Yakovlev’s teachings about the parity of telencephalic structures vs that of structures caudal to the telencephalon (Yakovlev 1948, 1963, 1968, 1970) remain of particular interest to anyone working in the field of neurolinguistics.

Yakovlev’s basic argument in this respect is that paired structures located caudal to the telencephalon emerge from two symmetrical anlagen - one left-sided and the other right-sided - belonging to the floor plate or to the roof plate of the neural tube, whereas the original anlage of the telencephalon is a single midline neuroblastic fountainhead located in the dorsal lip of the neuropore of His.

The cerebellar hemispheres, for instance, arise bilaterally, from anlagen located in the rhombic lips of the neural groove. Cerebellar neuroblasts thus migrate from these two symmetrical fountainheads and converge, dorsally and medially, until fusion occurs at the level of the vermis. The symmetry of the cerebellar hemispheres is therefore labelled as “primary symmetry” in Yakovlev’s lexicon.

Quoting Kingsburry (1922) as his source with regard to embryological events, Yakovlev goes on asserting that the telencephalon, unlike more caudal CNS structures, has neither a floor plate nor a roof plate but originally emerges from a part of the lamina terminalis embryonalis (lamina reuniens of His), a midline structure which, during the fourth gestational week, immediately after the emergence of the optic vesicles, grows on the midline and completes - but for the

anterior neuropore of His - the closure of the rostra1 end of the neural tube of the embryo, i.e. occludes its verticomedian slit.


Around the end of the fourth foetal week, the telencephalon is represented, immediately rostra1 to the optic vesicle, by a holosphere that is growing from the median fountainhead (located in the dorsal lip of the neuropore left open at the center of the lamina terminalis embryonalis). This holosphere is the anlage of the telencephalon as a whole but, more specifically, it is the anlage of the structures (including the septum, the para-olfactory areas, the olfactory bulbs and the hippocampi; Figure 2) which Yakovlev labels as “telencephalon impar” or “rhinic

brain”. According to him, the notions of parity and symmetry, and therefore those of right and left, have neither morphological nor functional significance with regard to telencephalon impar. He insists that the mode of projection of telencephalon impar is essentially ablateral, and teaches that it is related to “endokinesis”, or “cell-bound” movement (e.g. peristaltis, cardiac beats).

Around the sixth foetal week (when the embryo reaches seven or eight milli- meters in length), the rate of neuroblastic proliferation increases in the lateral aspects of the holosphere, thus causing the emergence of a first pair of evaginations; ventrally, these remain continuous over the midline. This first pair of evaginations constitutes the anlage of all but the rhinic telencephalon but, more specifically, it is the anlage of the structures (including the cingular gyrus, the isthmus, the para- hippocampal gyrus, the limen and the insula; Figure 2) which Yakovlev labels as “telencephalon semipar” or “limbic brain”. According to him, the notions of parity and symmetry, and therefore those of right and left, bear only limited morphological and functional significance with regard to telencephalon semipar. He insists the mode of projection of telencephalon semipar is ambilateral and teaches that it is related to “ereiskokinesis”, or “body-bound” emotional motility (e.g., pain, mimicry, swearing).

From around the ninth gestational week, neuroblastic proliferation becomes comparatively very active in the fundi of the first pair of evaginations and this results in the rapid growth of a second pair of evaginations dorsalaterally to the first one. This second pair of evaginations constitutes the anlagen of those neocortical telencephalic structures (including those of the frontal, parietal, occipital and temporal lobes; Figure 2) which Yakovlev labels as “telencephalon totopar” or

“supralimbic brain”. According to him, the notions of parity and symmetry, and therefore those of right and left, bear full morphological and functional significance only with regard to telencephalon totopar. He underlines the fact that only telencephalon totopar has a predominantly controlateral mode of projection and teaches that it is related to “telokinesis”, or “object-bound” voluntary motility (e.g. tool manipulation, articulated propositional speech).

In order to appreciate Yakovlev’s conception of parity and symmetry within the human brain, one therefore has to follow him in the opposition that he establishes between the “primary symmetry” of structures such as the cerebellar hemispheres

IEL 4:2-H


(cf. supra), which grow by convergence from two lateralized and symmetrical anlagen, and the “secondary symmetry” of structures such as the cerebral hemispheres which, in last analysis, emerge by divergence from a single median neuroblastic fountainhead, “as would two leaves of a (Yakovlev 1968).

TELENCEPHALON

IMPAR SEMIPAR

lotus from a common stem”

cl TOTOPAR

‘““--kJ - ANTBRIOR COUUISSURD

CINCULAR GYRUS

HIWOCAUPAL WlDIUINT)

CORnlS CALwsuY

Dl#NCEPHALON

HIPPOCAMIAL

Figure 2. Main Structures of Yakovlev’s Three Brains in the Adult. Black: Telencephalon impar. Dotted: Telencephalon semipar. White: Telencephalon totopar.

THE YAKOVLEVIAN TORQUE

Either because of dissociated rates in neuronal and/ or glial migration from the midline fountainhead and/or from secondary anlagen, or else because of post- migrational, i.e. of maturational phenomena such as would be, at the term of


synaptic competition, greater cellular elimination in a given cortical region as compared to its controlateral homologue, the supralimbic parity is, at least from the end of the seventh month of gestation, partly broken by regional asymmetries (Rosen and Galaburda 1985). Clearly, the best known such difference between homologue regions of the cerebral hemispheres is the one related to the speech area (Galaburda 1980; Galaburda er al. 1978a; Galaburda et al. 1978b) but these supralimbic asymmetries are often globally visible as a relative proeminence of the right prerolandic and left retrorolandic regions (Galaburda er al. 1978a), which represents part of the phenomenon that Yakovlev (1972) qualified as the “torque” of the human brain. As we will now see summarizing Yakovlev’s research on the ontogenesis of the corticospinal tracts, telencephalic asymmetry will secondarily determine asymmetry within caudal structures in which there existed no asymmetry to begin with, i.e. in structures belonging with zones of primary parity (cf. supra).

PYRAMIDAL DECUSSATION AND TRACTS

A topic which readily triggered Yakovlev’s gift of the gab was handedness, which he invariably associated to his conceptions concerning “telokinesis”, or “object- bound motility” (cf. supra). Thus, his 1963 presidential address at the eighteenth annual meeting of the Society of Biological Psychiatry focused on this topic (Yakovlev 1963). His manuscript opens on Aristophane’s assertion that Zeus had originally created man as a spherical entity, with eyes facing up to heaven and bottom firmly set on the ground, and that it was only at a later stage, after the creature had become proud and insolent, that the Thunderer split it, by way of punishment, into dimidiated hemispheres, with a right and a left side. In his con- cluding remarks, Yakovlev (1963) argues, that the “preferential lateralization of the spearhead action to one side of the plane of bilateral symmetry, or handedness, is a unique property of organization of the specifically human telokinesis” and he adds that there “is growing evidence that preferential, either ‘right’ or ‘left’, handedness in skilled acts of human ‘dexterity’ is one of the most recent products of evolution, indissolubly bound with . . . language.”

With Pasko Rakic, Yakovlev (1966) later published a shorter and more factual paper on the ontogenesis (as of the 16th gestational week) and morphology of the corticospinal tracts, i.e. of the axonal system which he considered to be the privileged centripetal pathway of telokinesis. Yakovlev and Rakic (1966) first report on their study of the pyramidal decussation in 100 foetal and neonatal brains, Their finding in this respect is that, in more than 85% of the specimens, the first bundle to cross the midline (1) comes from the left hemisphere’7 and (2) is bulkier than the immediately caudal bundle decussating from the right hemisphere; another finding is that, on the whole, more than two thirds of the specimens show a


RIGHT LEFT

PYRAMIDAL PATHWAY

Figure 3. Pattern of the Pyramidal Decussation and “Dominance” of the

Right Pyramidal Pathway at Cervical Level (According to Yakovlev and Rakic 1966).

greater number of fibers decussating from left to right than from right to left. Data on 130 foetal and neonatal cervical cords are then provided: in more than two thirds of the specimens, the number of direct pyramidal fibers is, at cervical level, greater on the right than on the left side. The authors summarize their observations by stating that “with regard to corticospinal (pyramidal) innervation, the right side of the spinal cord appears to be the preferred (‘dominant’) side” (Yakovlev and Rakic 1966). In another publication, Yakovlev (1972) reports on his study of the

pyramidal pathway in 105 adult specimens: “dominance” of the right cervical cord is present in 72 cases (80%); moreover, the few gross anomalies observed among the foetal specimens (total absence of decussation in three cases and, in another, total decussation from the left together with absence of decussation from the right) are not found among adult specimens 18. Yakovlev leaves it for his readers to ponder on

Paul Ivan Yakovlev and his Teaching 281

the eventual relationship between these data and the fact that most human beings are right-handed.

MYELOGENETIC CYCLES

Although he had long been interested in myelination and had indeed discussed it at some length in the context of an earlier paper on morphological criteria of brain growth (Yakovlev 1963) Paul Yakovlev was nearly 75 years of age when he published his classical paper on the subject (Yakovlev and Lecours 1967). This is where he put forward the original notion of “myelogenetic cycle” as a regional parameter of brain maturation and empirically defined it, for any given axonal system, as the period extending from the time of foetal or early postnatal appear- ance of stainableI myelin sheaths in that system to the age when its stained bulk and tinctorial intensity are comparable, under the dissection microscope to those in the normal adult brain.

Various fiber systems or regions may thus begin to myelinate early or late and, in either case, myelination can attain its apparent term more or less rapidly or slowly: among the specific radiations of the thalamus, for instance, the visual ones have a short cycle (Figure 4), the somesthetic a cycle of intermediate duration, extending from the ninth lunar month of gestation to about one and a half year postnatally, and the acoustic ones a cycle about three times longer than the latter (Figure 4); as to the nonspecific thalamic radiations, for instance those linking the pulvinar to the temporo-parietal cortex, they have a still longer cycle, with incipient myelination occurring about two months after birth and the process going on for about seven years thereafter before it is completed. Although he never thought in terms of cause-effect relationships, Yakovlev postulated that such differences in outset and duration of myelogenetic cycles somehow witnessed to a species-specific hierarchy of functional organization in the nervous system.

When he wished, usually in the context of Sunday-afternoon discussions at the Warren Anatomical Museum, to illustrate the interest of his “cycle” concept as a parameter of functional brain maturation, one of Paul Yakovlev’s favorite

examples was that of the myelogenesis of the pre-thalamic and post-thalamic acoustic pathways, which he opposed to myelogenesis of their optic counterparts (Lecours 1975). Both components of the latter, the retinogeniculate and the geniculocalcarine, display short cycles, completed in one rapid spurt between the eighth foetal and the fourth or fifth postnatal month (Figure 4). Optic myelogenesis is therefore precocious and brief, and it is monophasic. In sharp contrast, acoustic myelogenesis is biphasic: largely prenatal and very brief in the helicogeniculate component, where the cycle begins as early as the 2 I st foetal week and is completed up to collicular level at the 34th, and up to thalamic level around the third or fourth


postnatal month; long lasting and entirely postnatal in the geniculotemporal

component, where faintly myelinated fibers are first seen only at or around birth at

term, and where the cycle is not completed before the child is three to four years of

age (Figure 4). Yakovlev insisted that this sequence of events in anatomical

maturation closely parallels the timetable following which the two corresponding

sensory modalities enter into play as factors of behavioral development in the

human foetus and infant. Early during gestational life, the foetus is submitted to

gravitational (vestibular) and acoustic stimuli (movements of its own body,

external sounds such as voices and music, and sounds of maternal life - cardiac

beats, respiratory noises, borborigms and so forth - transmitted through the

amniotic sac and the maternal body walls, i.e. through structures which are

impermeable to photic information; in view of the precocity and shortness of the

pre-thalamic acoustic cycle, Yakovlev’s suggestion is that, during the earlier phases

of human life, the central apparatus for the intergration of such stimuli lays in the

tegmentum of the brainstem. Dramatic changes occur from the time of birth as to

the types of inputs that besiege the newborn’s central nervous system. On the one

hand, taught Paul Yakovlev, the relative importance of statoacoustic information

decreases greatly as the now omnipresent visual informations enter into play as

factors of behavioral development, and, if the short perinatal cycle of the retino-

cortical pathways is to be taken as a reliable indicator, rapidly assume a role which

will remain physiologically unchanged from infancy to maturity. Acoustic inform-

ations, on the other hand, assume a radically different role, soon to be largely

oriented toward speech acquisition; the existence of a chronological parallel is

therefore striking between the long period during which this acquisition takes place

and the protracted cycles not only of the post-thalamic acoustic pathway but also of

5m

------- I Birth

iv 2v 3V 4v

Figure 4. Myelinogenesis. Perinatal monophasic cycle of the optic

pathway (A: pre-thalamic. B: post-thalamic). Biphasic cycle of

the acoustic pathway (C: pre-thalamic, perinatal. D: post-

thalamic, postnatal and protracted).

Paul Ivan Yakovlev and his Teachings u19

the corticocortical associations between the acousticcorticesand other regions ofthe hemispheric surfaces (Yakovlev and Lecours 1967; Lecours 1975). Clearly, such parallels should be of interest to those contemporary researchers working in the domain of neonate cognition, especially with regard to the prelinguistic abilities of

the human newborn (Mehler and Fox 1985).

As mentioned above, the myelinogenetic cycles of non-specific thalamic radiations is late-blooming and long-lasting. The same is true of those long association bundles, whether commissural or intrahemispheric, especially those to and from non-specific association cortices such as that of the inferior parietal lobule. The longest cycles of them all, and Yakovlev never missed an occasion to give credit to Theodore Kaes (1907) for having provided convincing documents in this respect, are no doubt those of the intracortical neuropil within such non-specific association cortices: there, myelinogenesis does not seem to begin before several years after birth and it lasts several decades at least; as a matter of fact, and although he never wrote this to our knowledge, Yakovlevsometimes wondered whethercompletecessation of myelination within the non-specific association neuropil might be a marker of beginning cognitive involution. Clearly, such observations and parallels should be of interest to those contemporary researchers working in the domain of cognitive senescence and senility, especially with regard to the changes that occur in language abilities among the elderly (Obler and Albert 1980, 1984; Ulatowska 1985).

NOTES

1.

2. 3.

4.

5.

6.

7. 8. 9.

10.

Work supported by Grant 6178 of the Fonds de la recherche en santC du

Qubbec.

Faculte de Medecine, Universitt de Montreal. Centre de recherche, Centre hospitalier Cotedes-Neiges, 4565 Chemin Queen- Mary, Montreal, Quebec, Canada (H3W-1 W5). Although with modifications, this section is to a large extent excerpted from a previously published “In memoriam” (Lecours 1986). Direct quotes from Paul Yakovlev, printed in Italics, arefrominterviews led by Marjorie LeMay, Thomas Kemper or the author. Jacob Wylie: of Scottish origin, the founder of the Saint Petersburg Imperial Academy of Military Medicine, was physician to Catherine the Great and Surgeon General of the Russian armies until his death in 1834. Now Helsinki. Now Turku. Nobel prize in medicine and physiology, 19 13, for his discovery of anaphylaxis. Who succeeded Guillain in 1947 (Lhermitte et al. 1981).


II.

12. 13. 14.

And Henri Claude.

15.

16.

17.

18. 19.

“Which I must admit were flimsy indeed”, was later to add Paul Yakovlev. Who, Yakovlev insisted, was “the inventor of the rocket*‘. For instance, two cases of paraplegia in flexion of cerebral origin (Kemper 1984). Including to his homeland, Paul Yakovlev’s first trip back to Russiatookplace

in 1958, in the context of a U.S. scientific exchange mission to the U.S.S.R.; while in Leningrad, 39 years after he had left Saint Petersburg, a hostess wondered where on earth could an American scholar have learned to speak Russian exactly the way her grandmother used to. Several other voyages to Russia followed thereafter: renting a car in Paris and driving alone to Lenin- grad was something he utterlyenjoyedduringthe‘sixties’. Yakovlev’s travels to Russia included a period of several months of scientific work in Moscow, in 1978, as well as a farewell trip, in 1979, at the age of 83. “There is no other collection of neuroanatomical material in serial sections consistently fixed, embedded, cut, stained and mounted to such exacting standards [. . .] the Yakovlev Collection is an irreplaceable reference material, patiently collected over a period of 42 years” (Denny-Brown 1972, quoted by Kemper 1984). Yakovlev used to characterize this fact by saying that pyramidal axones from the left hemisphere have ‘the right of way”. Perhaps suggesting that such anomalies are not compatible with life. Using Loyez’ modification of Weigert’s haematoxylin stain (Bertrand 1930).

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Yakovlev - 1989 Obituary