Interesting that just as with brain evolution, brain anatomical knowledge also took place from the bottom up, with the cerebral sulci and gyri being the last structures to be understood!
1.1 The Cerebral Surface
Knowledge of brain anatomy in general and of its surface in particular is very recent. This is despite human interest in the brain being very old, with the making of cranial trepanations probably being the oldest systematized surgical procedure in our history (Sachs, 1952) and having been done successfully (on the basis of new bone growth after these procedures) in European Neolithic cultures about 10 000 years ago, and more frequently in South America by the pre-Inca and Inca cultures in Peru with findings that date until 2000 years ago (Finger, 1994; Graña et al., 1954; Lyons and Petrucelli, 1978; Sachs, 1952).
Figure 1.1 (A) Trephine skull opening from the Neolithic Period (Neolithic skull, Nogent-les-Vierges, Oise, France. Musée de l’Homme, Paris) (Sachs, 1952), and (B) trephine skull openings from the pre-Colombian Peruvian civilization, apparently with the aim of preserving bone over the superior longitudinal sinus (Graña et al., 1954).
The Egyptians were the first to provide systematic medical records with the writing of the Edwin Smith surgical papyrus (seventeenth century BC) based on the teachings of Imhotep (ca. twenty-seventh century BC), father of Egyptian medicine. The text deals particularly with traumatic lesions, but its hieroglyphics mention for the first time in history the equivalents for the words “brain” and “corrugations of the brain,” and also mention a note about a patient with an opened skull wound who became “speechless” during its palpation (Breasted, 1930 apud Catani and Schotten, 2012; Catani and Schotten, 2012). The Egyptians believed that the heart, and not the brain, was responsible for intellectual, emotional, motor, and sensation functions, and the brain was treated by them with indifference as also shown in the subsequent and much longer Ebers papyrus (Finger, 1994). Nevertheless, it is interesting to point out that, during their New Kingdom era, it was common to remove the brains of cadavers to be mummified through the nostrils and the base of the skull with the help of a small chisel and an iron hook (Finger, 1994), pioneering a trans-sphenoidal surgical route.
During antiquity, no significant contributions to neuroanatomy were made until the development of the Greek culture. Alcmaeon from Crotona (ca. fifth century BC) performed some of the earliest recorded dissections, described the optic nerves, identified that the sense organs were connected to the brain through nerves, and was the first to propose that the brain was the central organ of sensation and thought, which was also suggested by Anaxagoras (500–428 BC) at about the same time. Alcmaeon’s cephalocentric concept is known to have deeply influenced later philosophers and anatomists such as Pythagoras, Plato, Herophilus, Erasistratus, and Galen (Catani and Schotten, 2012; Debernardi et al., 2010).
Hippocrates (460–370 BC), the father of medicine, emphasized that the brain was responsible for mental activity and convulsions, although some important Greek philosophers of that time, like Aristotle (384–322 BC), the Stoics, and the Epicureans, still believed that the heart was the seat of intellectual, perceptual, and related functions (Finger, 1994).
Previously forbidden in Greek culture, human dissections began to be performed around 300 BC in Alexandria, Egypt, then a Greek city which was particularly culturally developed. There, Herophilus (ca. 335–280 BC), follower of Hippocrates and considered the father of anatomy, studied the brain, its ventricles, and the cerebellum, discriminated the motor from the sensitive nerves, and described the torcula of the cranial venous sinuses that bears his name (torcular Herophili). Erasistratus (ca. 310–250 BC), studying the comparative anatomy of the brain surface, already suspected a relationship between intellect and gyri complexity (Finger, 1994) and compared the arrangement of brain convolutions to the jejunum (Clarke and O’Malley, 1996).
With the decline of the Greek Empire, the Roman medicine that followed was largely a continuation of Greek ideas, particularly because many Greek physicians settled in Rome. Aurelius Cornelius Celsus (25 BC–AD 50), though not formally trained, practiced medicine and wrote the first Roman work De Medicina; however, it was Galen (AD 130–200) who left the best known anatomical contributions from this period (Finger, 1994; Singer, 1952; Sarton, 1954).
Galen was born in the Greek city of Pergamon, trained in Alexandria, and later settled in Rome where he was a surgeon for gladiators and performed dissections mainly on animals. Among all his anatomical contributions, in neuroanatomy, Galen numbered the cranial nerves and described the autonomic nervous system, but since most of his dissections and experiments were performed on cattle and on many other kinds of animal, he incorrectly considered that many of these findings were also pertinent to human anatomy (Sarton, 1954; Finger, 1994).
He followed Hippocrates in also rejecting Aristotle’s ideas that the brain simply served to cool the passions of the heart and in believing that the brain was also responsible for imagination, cognition, and memory (for Hippocrates, the basic components of intellect), but he did not believe that the convolutions of the brain were associated with intelligence as previously proposed by Erasistratus.
Galen believed that a natural spirit was produced in the liver, converted in the heart to a higher form, named the vital spirit, and was then carried to the brain through the carotid and rete mirabile (“wonderful net”). This is a vascular plexus located at the base of the brain as observed by him in the dissections of some animals, particularly of oxen (Clarke and Dewhurst, 1975; Finger, 1994; Singer, 1952). It was then transformed into animal spirits within the brain ventricles as already proposed previously by Herophilus of Alexandria almost five centuries before (Dobson, 1925 apud Catani and Schotten, 2012).
The Church fathers of the fourth and fifth centuries adopted Galen’s ideas associating the higher human functions mostly with the brain ventricles. One of the earliest advocates of the so-called ventricular theory of brain functions was Nemesius, Bishop of Emesa, a city in current Syria, and others that followed him in this period related the ventricular cavities with different functions (Clarke and Dewhurst, 1975; Finger, 1994), generating conceptions that lasted for many centuries.
The approximately 1000 years of the Middle Ages, roughly from the fourth to the fourteenth century, as is well known, were poor regarding scientific developments in general. Although having had the contributions of Avicenna (AD 980–1037) in the Arabic world who is credited with the first representation of the brain around the year AD 1000 by some authors (Tamraz and Comair, 2000), and the contributions of the first European human dissections by Mondino dei Luzzi (ca. 1270–1326) (Finger, 1994; Lyons and Petrucelli, 1978; Tamraz and Comair, 2000), anatomical studies were very limited, in particular because human cadaveric dissections were forbidden at that time.
The relative liberation of this practice that occurred during the Renaissance finally led to the progressive development of all anatomical knowledge, and the most preeminent figure in this field was undoubtedly Andreas Vesalius (1514–1564), professor of anatomy and surgery at Padua University, Italy.
Vesalius was a native of Brussels who studied anatomy in Paris with Jacobinus Sylvius (1478–1555), and his seminal work De Humani Corporis Fabrica (On the Working of the Human Body) (Saunders and O’Malley, 1950) was completed in Padua and Venice in 1542. It was published in Basel in 1543 (Finger, 1994; Singer, 1952) with the artwork probably done by Jan Stephan van Calcar (ca. 1499–1546) and/or by other students of the great painter Titian (ca. 1487–1586). The Fabrica was based on extensive human dissections, and Vesalius was particularly led to indicate Galen’s anatomical errors, having counted some 200 of them. In 1544, Vesalius left Italy to become court physician to Charles V (1500–1558), which ended his career as an anatomist (Finger, 1994).
Vesalius left many contributions to neuroanatomy, with descriptions of the meninges, cerebral hemispheres distinguishing the white and gray matter, corpus callosum and septum pellucidum, ventricles, fornix, colliculi, and pineal gland, cerebellar hemispheres and vermis, infundibulum and pituitary body (Lyons and Petrucelli, 1978; Saunders and O’Malley, 1950; Singer, 1952; Tamraz and Comair, 2000). With regard to the cerebral gyri, Vesalius still illustrated them chaotically and understood their shape and folding to be responsible for anchoring the vessels that penetrate the brain through the sulci (Vesalius, 1543 apud Catani and Schotten, 2012).
Although having denied the existence of the rete mirabile in humans, Vesalius did not reject entirely the ideas defended by Galen and the ventricular localization theory itself, and this major interest in the ventricular cavities may explain the relative neglect of the brain gyri by all the anatomists throughout more than 20 centuries.
Other contemporaneous authors of this period were the great artist and also anatomist Leonardo da Vinci (1472–1519), who besides his well-known studies of the brain ventricles also made beautiful but incorrect illustrations of the cerebral surface (Cianchi and Breschi, 1997; Clayton, 1992), and Julius Casserius (ca. 1545–1616). His work represented the brain convolutions, which at that time were still understood to resemble the small bowel as described previously by Herophilus and by Erasistratus 18 centuries before (Singer, 1952).
Constanzo Varolio (1543–1575) started slicing the brain and described the pons in 1573 (Varolio, 1573 apud Clarke and O’Malley, 1996), and in 1587, Giulio Cesare Aranzi (1530–1589) described the hippocampus within the lateral ventricular cavity (Varolio, 1573 apud Clarke and O’Malley, 1996).
In 1663, Franciscus de le Boë (1614–1672), also known as Dr. Sylvius, described the lateral cerebral sulcus (Sylvius, 1663 apud Catani and Schotten, 2012), which came to be named the Sylvian fissure by Caspar Bartholin (Bartholin, 1641 apud Catani and Schotten, 2012; Catani and Schotten, 2012) in 1641. For some authors, the Sylvian fissure was primarily described by Girolamo Fabrici d’Aquapendente (ca. 1553–1619) (Collice et al., 2008), who followed Andreas Vesalius (1514–1564) and Gabriel Fallopius (1523–1562) at the University of Padua (Finger, 1994).
In 1664, Thomas Willis (1621–1675) published his highly regarded Cerebri Anatome, which featured illustrations by the renowned architect Christopher Wren (1632–1723). In addition to describing the group of arteries surrounding the base of the brain now known as the circle of Willis, he introduced a variety of terms, including neurology, hemisphere, corpus striatum, peduncle, and pyramid, and related the cerebral gyri to memory, but still not representing the brain gyri and sulci properly. Interestingly, Willis related the striatum with movement and sensation, and the corpus callosum with imagination (Finger, 1994).
Raymond Vieussens (1644–1716) published the famous Neurographia Universalis in 1690 (Vieussens, 1690), describing in detail the centrum semiovale and other cerebral structures, but still illustrating the brain surface similarly to the small bowel (Finger, 1994; Tamraz and Comair, 2000). Godefroid Bidloo clearly displayed the central sulcus in his atlas and textbook published in 1685 (Tamraz and Comair, 2000), and subsequently Félix Vicq d’Azyr (1748–1794), famous for describing the mammillothalamic tract, also described the precentral and postcentral convolutions separated by the central sulcus, and coined the term uncus (Tamraz and Comair, 2000). In 1809, Johann Christian Reil (1759–1813) provided a comprehensive description of the insula (Lockard, 1977), which had already been identified by Bartholin in 1641 (Finger, 1994; Tamraz and Comair, 2000). In 1827, Herbert Mayo, student of the renowned anatomist and surgeon Charles Bell (1774–1842), published illustrations of the corona radiata and internal capsule, as well as other important tracts (Türe et al., 2000). In 1829, the Italian anatomist Luigi Rolando (1773–1831) published his text Della Struttura degli Emisferi Cerebrali (Rolando, 1829 apud Türe et al., 2000), becoming the first author to accurately portray the central sulcus, which is still also referred to as the fissure of Rolando (Finger, 1994; Tamraz and Comair, 2000).
Figure 1.2 Illustrations of the cerebral surface from the Renaissance: (A) by Andreas Vesalius (1514–1564), (B) by Giulio Casserio (ca. 1545–1616), (C) by Raymond Vieussen (1641–1716), and (D) by Franciscus de le Boë, known as Dr. Sylvius (1614–1672) already depicting the lateral fissure that bears his name.
In the early nineteenth century, Frans Joseph Gall (1758–1828) related the different brain convolutions to different mental faculties and “propensity,” adopting the concept of organology where each brain convolution corresponded to a specific organ. For Gall, each gyrus would cause an impression on the skull, generating an external protrusion that would express each individual character (Clarke and Dewhurst, 1975; Gall and Spurzheim, 1810–1819 apud Catani and Schotten, 2012). Although not justified at all, Gall’s concepts, altogether known as phrenology, encouraged the investigation of cortical localizations and hence the clinico-anatomical correlation method (Catani and Schotten, 2012).
Achille Loius Foville (1799–1891) was the first author in the history of neuroanatomy to illustrate perfectly the sulci and gyri of the brain surface, in his atlas of brain anatomy edited in 1844, but did not describe their organization within the text (Brogna et al., 2012).
It was the German physiologist Friedrich Arnold (1803–1890) who first used the terms frontal, parietal, and occipital to describe the cranial bones. In a text published in 1851 (Broca, 1876b), Arnold recognized only the Sylvian fissure and the parieto-occipital sulcus (then known as the internal perpendicular fissure) (Déjérine, 1895) as anatomically constant sulci, and he described the temporal region as an anterior extension of the occipital region.
It is notable that, despite the intense interest that humankind has always had in relation to the brain, it was only in the middle of the nineteenth century that the general anatomical organization of the cerebral sulci and gyri was perceived and described by the French anatomist Louis Pierre Gratiolet (1815–1865) who succeeded his professor Francois Leuret (1797–1851) (Leuret and Gratiolet, 1857–1959 apud Türe et al., 2000; Gratiolet, 1854 apud Pearce, 2006; Pearce, 2006). In addition to his well-known description of optic radiation, Gratiolet together with Leuret also distinguished between primary and secondary sulci based on their phylogenetic appearance, adopted the terms initially proposed by Arnold to divide each cerebral hemisphere into lobes, and coined the elegant term “plis de passage” to describe the connections between adjacent gyri. Gratiolet was the first anatomist to understand and describe the fact that, despite individual variations, the cerebral sulci and gyri are organized in accordance with a general arrangement (Gratiolet, 1854 apud Pearce, 2006; Pearce, 2006).
In relation to his original concept of brain lobes, it is interesting to point out that regarding the precentral and postcentral gyri, Gratiolet initially considered the former one, then called the “first anterior ascending gyrus” (Déjérine, 1895), as belonging to the parietal lobe (Gratiolet, 1854 apud Pearce, 2006), and only a few years later decided to consider it part of the frontal lobe, leaving the latter, then called the “second anterior ascending gyrus” (Déjérine, 1895), part of the parietal lobe (Leuret and Gratiolet, 1857–1959 apud Türe et al., 2000).