Department of Neurosurgery, St Elisabeth-Tweesteden Hospital, Tilburg, The Netherlands
In 2009, Craig Bennett and his co-workers put a mature Atlantic salmon in an MRI scanner and showed it a series of photographs . The (dead) salmon had been instructed to determine the emotion of photographed people during MR scanning. Much to everybody’s surprise, three activated areas were found exactly in the brain cavity of the salmon, as shown in Fig. 1.1. The results of this experiment were presented at a human brain mapping conference in Toronto . Statistically speaking, the images made a strong point that the salmon was engaged in a cognitive task. The poster, of course, argued differently and pointed to the dangers of modern functional neuroimaging techniques.
Type in ‘phrenology’ on the Internet and you will quickly find a vast number of beautiful images such as the one shown in Fig. 1.2. This image illustrates the phrenologists’ idea that the mind consists of several different ‘organs’ or ‘faculties’ that each harbour a specific mental quality. A broad range of human qualities was covered, as variable as benevolence, amativeness, causality or language. Phrenologists associated these mental qualities with specific locations in the brain. This was a radically new concept in an era where philosophical and religious thinking was dualistic in nature and still considered the mind or soul to be undivided, immaterial and immortal. Of course, they were wrong on the details. It is easy for us to criticize the fact that they confined complex behavioural functions to specific brain regions. However, it is often forgotten that the phrenologists paved the way for future neurological and neuropsychological theories about brain function. They were the first to associate brain functions with particular locations in the brain, still the most commonly accepted localist view in clinical practice. The phrenologists were particularly criticized for the fact that they assumed that the strength of a brain function scaled with its physical properties. They considered the size of the organ proportional to its mental power, and the skull to reflect the underlying size of the organ. Samuel Wells (1888) put it as follows in the introduction of his book How to Read Character :
Phrenological representation of brain functions(Figure taken from Samuel Wells’ How to Read Character, 1888)
Now, as is the soul which is incarnate in it, so is the brain in texture, size and configuration; and as is the brain, so is its bony encasement, the cranium, on which may be read, in general forms and special elevations and depressions, and with unerring certainty, a correct outline of the intellectual and moral character of man.
It is of course impossible to pick out one point in history where the phrenological ideology started. The fact is that it was ridiculed from the beginning and that the term has often been used with a negative connotation. However, the ghost of phrenology still haunts neuroscience. Examples are easily taken from recent studies that have investigated the relationship between brain structure and function. The results of some of these scientific papers made it to the popular press, and this resulted in remarkable headings such as ‘Political Views Reflected in Brain Structure’ (www.abcnews.go.com) or ‘What’s in Voters Heads. Brain Scans Reveal Clues’ (www.seattlepi.com). This happened, for example, to the studies of Amodio and colleagues (2007) . They described a relationship between liberalism and brain activity in the anterior cingulate cortex and published this in 2007 in the journal Nature Neuroscience under the title ‘Neurocognitive Correlates of Liberalism and Conservatism’. Here is their abstract :
Political scientists and psychologists have noted that, on average, conservatives show more structured and persistent cognitive styles, whereas liberals are more responsive to informational complexity, ambiguity and novelty. We tested the hypothesis that these profiles relate to differences in general neurocognitive functioning using event-related potentials, and found that greater liberalism was associated with stronger conflict-related anterior cingulate activity, suggesting greater neurocognitive sensitivity to cues for altering a habitual response pattern.
Others found that ‘this functional correlate of political attitudes has a counterpart in brain structure’ . Kanai and colleagues (2011) reported that liberals had a larger area in the anterior cingulate cortex and conservatives had a larger right amygdala . Both these areas are part of the limbic system that deals, amongst others, with emotional processing; the amygdala is specifically associated with responses to fear.
In expert hands, the modern imaging techniques have revolutionized neuroscience. However, these techniques are complex. The measured signals are noisy, and analysis and interpretation can be difficult and are certainly less straightforward than these news headings falsely imply. Quick and dirty conclusions are easily drawn, but not often justified. Of course, the phrenological part of all this lies in the proposed hypotheses and interpretation of the results, not in the technique itself. It is not very difficult to get false-positive findings in individuals or groups with functional imaging techniques; but even with very strict methodological protocols, one can get surprising results, as the fMRI experiment with the salmon showed.
Franz Josef Gall (1758–1828) is considered the founding father of phrenology and cranioscopy (the ‘reading’ of the bumps on the skull). Even in his own time, he received a lot of discredit for his ideas, and he was exiled from Vienna, whereupon he moved to France in the hope of finding a more responsive scientific environment (which he did; he became a well-known figure in his time). Still it is fair to say that Gall made a historical and classical contribution to the concept of cerebral localization. See for a thorough overview Young’s brilliant book Mind, Brain and Adaptation in the Nineteenth Century . What was revolutionary in itself, and a great contribution to psychology, was the fact that Gall considered behaviour and brain functioning amenable to objective observation. He based his discovery of the 27 faculties on empirical examinations and used several different methods to do this. He collected measurements and casts or skulls of several hundred heads and also made a large number of observations on the crania and behaviour of animals. According to Young (1970), ‘he travelled to schools, foundling homes, hospitals, prisons and lunatic asylums, and obtained information on remarkable heads and remarkable talents wherever he could’ . As counter-proof, Gall also examined individuals with minor qualities for a lack of the corresponding cranial prominence.
Gall and his later followers made a number of suppositions on which their theories were based. Despite the fact that Gall, together with Spurzheim, did extensive and important work in neuroanatomy (e.g. they postulated that white matter served a conduction function and described the anatomical decussation of the pyramids), he considered this work irrelevant for his organology and was convinced that knowledge of functions preceded that of the anatomy of the brain . This discrepancy remains something of a mystery, as Gall was well aware of neurological data from victims that had suffered head and brain injuries. He even described such cases himself. Gall stated his main assumptions already in 1798 in a letter to Baron von Retzer, before he did much of his anatomical work .
Here are the ‘chief principles of phrenology’, as formulated in 1868 by another phrenologist, Samuel Wells, ‘every one of which is supported by an array of unquestionable facts and susceptible to the clearest proof’ . Note that this is almost 50 years after Gall’s death and in an era where Broca and Wernicke already based their theories on postmortem examination of damaged brains.
The brain is the organ of the mind.
Each faculty of the mind has its separate or special organ in the brain.
Organs related to each other in function are grouped together in the brain.
Size, other things equal, is the measure of power.
The physiological conditions of the body affect mental manifestation.
Any faculty may be improved by cultivation and may deteriorate through neglect.
Every faculty is normally good, but liable to perversion.
Although Wells motivates these principles with a list of ‘obvious’ facts and findings, he fails to give scientific proof (from our modern point of view). Some arguments are valid from a rational point of view, for instance, when he states that ‘Partial injuries to the brain result in suspension of one or more faculties, while others retain their normal activity, which could not be the case if the brain were a single organ’ .
Opposed to the localist theories of Gall and later Broca and several others, there are the field theories that hold that the brain acts as a single equipotential unit. Jean Pierre Flourens (1794–1867) is considered by many the modern founder of the field theory. He was the first to base his work on experiments with animals from which he systematically removed parts of the brain and observed the resulting disturbed behaviour. In a famous paper from 1824, he describes several of these ablative experiments. Note that in that time little was known of brain anatomy; the only parts that were distinguished were the medulla, the corpora quadrigemina, the cerebellum and the hemispheres. There was no knowledge of white and grey matter.1 Also, bear in mind that the methods of stimulation and ablation were probably too crude to reveal much information on localization of function . Details of the surgical procedures and behavioural observations are not given to the extent that experiments can be repeated. The following excerpts are all from Flourens’ 1824 paper, taken from the book Readings in the History of Psychology (1948) .
The entire cranial portion of a young dog was removed. I pushed a needle through the cerebral lobes, cut them in all directions, and also cut through the cerebellum on that side. The animal seemed neither disturbed nor agitated.
I removed both cerebral hemispheres of a pigeon, including the optical layers. The iris retained all of its ability to contract. However, I had only to push through the optic nerves or the corpora quadrigemina to elicit strong and prolonged contractions.
This experiment was repeated on several pigeons. The result was always the same.
Consequently the cerebral hemispheres are not responsible for muscular contractions.
Flourens describes several other experiments with rabbits but mainly with pigeons (!) from which he concludes that ‘the cerebral lobes are neither the origin of muscular contractions nor are they the origin of the control of movements (…), but it also seems demonstrated that they are the exclusive origin of volition and sensation’. Flourens had noted that without both cerebral lobes pigeons kept intact reflexes but lacked spontaneous movements. Further on he notes:
One can remove, from the front, or the back, or the top or the side, a certain portion of the cerebral lobes, without destroying their function. A small part of the lobe seems sufficient to exercise these functions.
After certain limits have been surpassed, they are entirely extinguished. The cerebral lobes concur than in their entirety with all of their functions.
Finally as one sensation is lost completely, all of them are. Consequently there is no different origin for any of the faculties nor for any of the sensations.
Interestingly, Flourens also describes recovery of function after damage to the brain. He notes that after some of the removals, the animals regain most or all of their functions.
We have just seen that is possible to remove a certain portion of the cerebral lobes without destroying their functions completely. However, there is more than that. The lobe can recover these functions in their entirety after having lost them completely.
Flourens describes the complete recovery of functions in a pigeon when he stops ablation as soon as the animal ‘had lost completely the use of all senses and intellectual functions’. Recovery takes a period of 6 days, in another case it takes 15 days. When he pushes the resection further, he notes that the animals fail to make a complete recovery. Flourens concludes that:
as long as not too much of the lobes is removed, they may regain in due time the exercise of their functions. Passing certain limits, however, the animal regains them only imperfectly and passing these new limits, it does not recover them at all. Finally, if one sensation comes back, all come back. If one faculty reappears, they all reappear.
Similar recoveries are seen when Flourens removes parts of the cerebellum or corpora quadrigemina. He ends his paper with the conclusion that:
When one point in the nervous system becomes excited, it excites all others; one point irritated, irritates all. There is community of reaction. Unity is the great reigning principle; it is everywhere; dominates everything. The nervous system is then only one single system.
Flourens related loss of function to the extent of damage, and hereby adopted a holistic concept . His theories were perfectly in line with contemporary philosophical assumptions and remained the dominating view in the first half of the nineteenth century. His experimental work on the brain as a unitary sensorium was used to refute phrenological theories whereby other incompatible observations were disregarded. Tizard refers to two of these observations in a review paper . One was courtesy of Charles Bell (1774–1842), known from several discoveries that bear his name such as Bell’s palsy. He indicated that when separate nerve tracts lead to separate areas in the cortex, these areas therefore must have distinct functions. The other was from François Pourfour du Petit (1664–1741) whose experiments were particularly remarkable. This French surgeon first made a number of postmortem observations in patients with a hemiplegia and a contralateral brain lesion. Then he did ablative experiments with dogs and established a relationship between damage in one hemisphere and a consequent paralysis on the opposite side . Almost a century later, Dominique Jean Larrey (1766–1842), another French (military) surgeon and a contemporary of Flourens and Gall, described 12 patients with speech difficulties, most of whom had traumatic brain injuries. His work has been described in a number of books and papers . One of Larrey’s patients was a corporal in Napoleon’s army who was struck by a musket ball in the left eyebrow at Waterloo, resulting in a depressed skull fracture and brain injury. The soldier, Louis Manez, was left with a right hemiplegia and language deficits. Despite his wound he partially recovered and regained mobility to such an extent that he could return to the army where he became a sergeant instructor. Manez compensated for his remaining naming problems by reading from lists and instruction booklets. It is interesting to know that Larrey consulted with the famous Gall on several of his patients and that Gall included some of these patients in his own works to support these ideas . The skull of Manez was placed in what is now the museum of Natural History in Paris (see Fig. 1.3).
The skull from 24-year-old soldier Louis Manez who suffered a gunshot wound and skull fracture in the left frontal region at Waterloo in 1815. The patient recovered from a hemiparesis but retained most of his language problems. Outside view (left) and inside view (right) (Figure taken from Jellinek, 2002)
1.3 Bouillaud and Broca
Paul Broca (1824–1880) is credited for the discovery of a language area that now bears his name. In his famous paper from 1861, he located ‘the seat of the faculty of spoken language’ in the third frontal convolution on the left side of the brain, near the coronary suture . Modern neuropsychology and neurology mark this discovery as the beginning of the era of localization of function in the brain, but the story of Broca’s area is much more complex and involves many other researchers. As Young (1990) begins in his chapter on Broca:
Broca’s localization of a centre for ‘the faculty of articulate language’ was the first localization of function in the hemisphere that met with general acceptance from orthodox scientists. Consequently, Broca is usually credited with priority in initiating the modern doctrine of cerebral localization. This citation has appeared with such regularity that this fact alone gains for it a species of historical truth. However, if one begins to examine his claim to priority, it is difficult to establish with any degree of certainty. His work is part of a continuous consideration of aphasia and cerebral localization that directly stems from Gall and was a live issue throughout the intervening decades. Neither the concept of a faculty of articulate language nor its localization in the frontal lobes was new .
Before Broca, several others had already demonstrated patients with speech deficits and focal lesions. According to Whitaker, ‘literally hundreds’ of case reports had been published in medical or phrenological journals from the 1820s onward, either with or without evidence from postmortem examinations . Therefore, the practising medical doctor must have been aware of the circulating doctrine of a frontal lobe speech centre . One of them was Jean-Baptiste Bouillaud (1796–1881), born a generation before Broca and to become professor of medicine and head of la Charité hospital in Paris. Bouillaud was one of the few remaining followers of Gall’s phrenology in the academic world, but advocated a different and more scientific methodology: he was convinced that observation of the brain was always essential, and he sought correlation between clinical symptoms and brain lesions. Gall, as we have seen before, ‘explicitly said that inspection of brains and “accidental mutilations” (pathological lesions) played a subordinate role in confirming localizations which he had discovered by his cranioscope methods’ . In 1825, Bouillaud published his Clinical studies—showing that the loss of speech corresponds to a lesion of the anterior lobes of the brain—a confirmation of M. Gall’s view regarding the seat of the organ of articulate speech . Gall had positioned the language faculty on the floor of the orbit in the lower part of the frontal lobes. He supposedly did this after initial observations made in childhood of classmates who could easily learn verbal material by heart and had ‘large prominent eyes’. After Gall observed several others of these correlations, he concluded that the area for ‘recollection of words or verbal memory’ must lie directly behind the eyes and was prominently large in these subjects. Bouillaud was less specific on the exact location of the speech centre and argued on the basis of clinical evidence that loss of speech must be due to a lesion in the frontal lobes; he did not refer to convolutions nor to a specific hemisphere. He was a fierce opponent of theories of equipotentiality and debated amongst others with Flourens.2
No physician who is in the least familiar with clinical studies has failed to observe many defects in locomotor functions produced by an illness of the brain. The inflammation causes spasmodic movements, cerebral compression, more or less widespread paralysis. It is therefore not without a good deal of astonishment that we read in the works of M. Flourens (…) that the brain exerts no immediate and direct influence on the muscular system .
Bouillaud proposed not only centres in the brain for movements of the limbs but for all organs that related to muscular movements, such as the tongue and the eyes. He deduced from case studies that ‘paralysis of the speech organs can exist independently from other paralysis’ . He also made a distinction ‘between the ability to produce words as signs of ideas while preserving their memory—and the ability to articulate these same words. There exists, as it were, an internal and external speech the latter is only the expression of the former’ . This relates to our current clinical distinction of dysphasia and dysarthria. Bouillaud even presented remarkable in vivo evidence when he had the opportunity to study the brain of a patient with a gunshot wound and a skull defect over the frontal lobes.
Curious to know what effect it would have on speech if the brain were compressed, we applied to the exposed part a large spatula pressing from above downwards and a little from front to back. With moderate pressure, speech seemed to die on his lips; pressing harder and more sharply, speech not only failed but a few words were cut off suddenly .
So why is it that modern neuropsychology considers theories of cerebral localization to begin in 1861 with the observations of Broca and not, for instance, with those of Bouillaud at some earlier time? If one reads Broca’s original paper, it is rather remarkable that it made such a historical impact. But, as always, one has to take the circumstances into account, and in 1861, localism was reconsidered more with an open mind than was done in the decades before. In that year, the Societé d’Anthropologie (of which Broca was founder and secretary) held a series of debates on localization of function with Gratiolet arguing in favour of holism and Auburtin (pupil and son-in-law of Bouillaud) in favour of localism. During the debate, Auburtin promised to abandon his belief in cerebral localization if anyone could produce a case of loss of speech without a lesion in the anterior lobes of the brain. Precisely at that time, in April 1861, the patient Leborgne had come under the surgical attention of Broca because of a gangrenous infection of his right lower extremity. The 51-year-old Leborgne had already been in the Bicêtre hospital for 21 years because of speech problems and a hemiparesis. Despite his epilepsy, he had been a miller until at the age of 30 ‘he lost the ability to speak’ . Broca was unable to discover retrospectively whether this loss of speech had an acute or a more gradual onset and whether there were accompanying symptoms at the time. Leborgne was known as ‘Tan’ because the only thing he said in response to questions was ‘tan tan’, accompanied by ‘varying movements with which he was able to express most of his ideas’. He quickly got angry when people did not understand him and was thought to be egoistical, vengeful and mean according to Broca’s case report. Ten years after he lost his speech, Leborgne gradually developed a right-sided hemiplegia, starting with the muscles of the arm and gradually spreading to involve his leg and making him bedridden. The exact diagnosis has never been made and remains something of a riddle; Broca speaks of a ‘chronic and progressive softening’. Broca remarks that the examination of this patient was difficult because of his inability to speak and to move the right side of his body; furthermore, Leborgne was ‘in such a perilous state that it would have been cruel to have tortured him with long examinations’ . Still, considerable neurological details are given in his paper:
The tongue was absolutely free; it was not deformed in any way; the patient could move it in any direction and stick it out of his mouth. The two halves of the organ were of the same thickness. The difficulty in swallowing I mentioned, was due to a paralysis, which was beginning at the pharynx, and not due to a paralysis of the tongue, as it was hard to swallow the third time. The muscles of the larynx did not seem to be altered, the timbre of the voice was natural, and the sound the patient produced, to pronounce his monosyllables, was completely pure.