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Neurologic-Psychiatric Syndromes in Focus - Part I
J. Bogousslavsky
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Neurologic-Psychiatric Syndromes in Focus - Part I
J. Bogousslavsky
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Bogousslavsky J (ed): Neurologic-Psychiatric Syndromes in Focus. Part I â From Neurology to Psychiatry. Front Neurol Neurosci. Basel, Karger, 2018, vol 41, pp 77â89 (DOI: 10.1159/000475721)
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The KlĂźver-Bucy Syndrome
Douglas J. Lanskaa, b
aVA Medical Center, Great Lakes VA Healthcare System, Tomah, WI, and bDepartment of Neurology, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA
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Abstract
In 1937, Heinrich KlĂźver and Paul Bucy described a dramatic behavioral syndrome in monkeys after bilateral temporal lobectomy. The full KlĂźver-Bucy syndrome (KBS) â hyperorality, placidity, hypermetamorphosis, dietary changes, altered sexual behavior, and visual agnosia â is evident within 3 weeks following operation. Some KBS features (i.e., hyperorality, placidity, hypermetamorphosis) persist indefinitely, whereas others gradually resolve over several years. KlĂźver and Bucy were initially unaware of an earlier report of KBS by Sanger Brown and Edward Schäfer in 1888. Human cases were recognized in the 1950s, as surgeons employed bilateral temporal lobectomies to treat seizures. Various attempts were made to localize the component features to specific areas of the temporal lobe, with mixed success. Bilateral ventral temporal ablations and bilateral temporal lobectomies produced marked impairment in visual discrimination, whereas lateral resections or unilateral lesions did not. Discrete bilateral lesions of the lateral amygdaloid nucleus produced a permanent âhypersexed state.â By the 1970s, it was clear that the major symptoms of KBS are produced by destroying either the temporal neocortex or the amygdala bilaterally. KBS is now thought to be caused by disturbances of temporal portions of limbic networks that interface with multiple cortical and subcortical circuits to modulate emotional behavior and affect. The clinical features of KBS in man are similar to those in monkeys, but the full syndrome is rarely seen, probably because the anterior temporal lobe dysfunction is usually less severe than that following total temporal lobe ablation in monkeys. Human KBS does not occur in isolation, but is typically part of a complex behavioral syndrome that almost always includes amnesia and aphasia, and that may also include dementia and seizures. The treatment of KBS is difficult and often unsatisfactory.
Š 2018 S. Karger AG, Basel
Introduction and History
In 1937, German-born American psychologist Heinrich KlĂźver (1897â1979) and American neurosurgeon and neuropathologist Paul Clancy Bucy (1904â1992) described a dramatic behavioral syndrome in Rhesus monkeys that had undergone bilateral temporal lobectomy [1â13]. This was an unanticipated consequence of KlĂźverâs studies of the reactions of humans and animals to mescaline, a naturally occurring psychedelic alkaloid similar in its effects to LSD.
In an obituary of KlĂźver, fellow psychologist William A. Hunt (1903â1986) recounted how KlĂźver became bored after a few days away from his laboratory while on vacation on a New Hampshire farm:
[KlĂźver] began investigating the effects of mescal on the farmerâs cow. He overestimated the ameliorating effects of body weight on dosage size and the cow died. KlĂźver confessed his guilt and reimbursed the farmer, but as KlĂźver said, âHe took it unpleasantly.â KlĂźver also used himself as a subject and consequently suffered an attack of mescal poisoning that left him seriously ill for a while [11, p 160].
As noted in a later biographical memoir, while KlĂźver was âat the University of Minnesota around 1924, he ingested mescal buttons and compulsively documented the nature of his own experiences during intoxicated statesâ [13]. KlĂźverâs later work with mescaline produced behavioral manifestations in monkeys that suggested to him that this drug might act on the temporal lobe:
Our interest in temporal lobe functions was aroused by the discovery of one of us (KlĂźver) that the injection of mescaline or chemically related substances into monkeys produces peculiar chewing and licking movements as well as convulsions, in other words, symptoms resembling those found in the âuncinate group of fitsâ described [in 1899] by [English neurologist John] Hughlings Jackson [1835â1911] and [Scottish neurologist James Purves] Stewart [1869â1949]. It was thought desirable, therefore, to remove the temporal lobes, including the uncus [3, pp 989â990].
On this basis, KlĂźver induced Bucy to perform staged bilateral temporal lobe resections on monkeys to assess whether the effects of mescaline would be ameliorated. On December 7, 1936, Bucy removed most of the left temporal lobe of an aggressive adult female Rhesus monkey named âAuroraâ [7, 10, 13]. As Bucy later recounted, the following morning KlĂźver called him on the telephone and abruptly demanded to know, âWhat did you do to my monkey?â [10]. Bucy hurried to the office and observed that the once-aggressive monkey had become âtame,â a behavioral change that was even more pronounced after Bucy removed the opposite temporal lobe in a subsequent operation on January 25, 1937 [7, 10, 13].
The initial report by KlĂźver and Bucy in April 1937, presented at the annual meeting of the American Physiological Society in Memphis, Tennessee, described the effects of sequential staged bilateral temporal lobectomy in an adult Rhesus monkey:
The animal does not exhibit the reactions generally associated with anger and fear. It approaches humans and animals, animate as well as inanimate objects without hesitation and although there are no motor defects, tends to examine them by mouth rather than by the use of hands. There is a general slowing down of movements; the quick, jerky movements characteristic of the normal Rhesus monkey have almost entirely disappeared [1, p 352].
Although the monkey had no impairment in visual acuity or in the ability to visually localize the positions of objects, it seemed unable to recognize objects by sight:
Table 1. KlĂźver-Bucy syndrome in monkeys
Permanent manifestations |
1Hyperorality (marked oral examination of objects with licking, sucking, chewing movements, and placing of non-food objects in the mouth) |
2Placidity |
3Hypermetamorphosis (constant manual exploration and inappropriate attention to new stimuli) |
Temporary manifestations |
4Dietary changes (hyperphagia, pica, coprophagia) |
5Altered sexual behavior (autosexual, heterosexual, homosexual) |
6Sensory agnosias (âpsychic blindnessâ) |
The hungry animal, if confronted with a variety of objects, will, for example, indiscriminately pick up [various objects, including uncharacteristically a live snake]. Each object is transferred to the mouth and then discarded if not edible. ⌠These symptoms of what appears to be âpsychic blindnessâ are not present in four other monkeys ⌠in which only one temporal lobe has been removed [1, p 353].
As KlĂźver and Bucy subsequently elaborated, the full KlĂźver-Bucy syndrome (KBS) â hyperorality, placidity, hypermetamorphosis, dietary changes, altered sexual behavior, and visual agnosia (Table 1) â is evident within 2â3 weeks following operation [3, 5, 6]. Hyperorality was manifest by a marked tendency to place non-food objects in the mouth, and to examine objects orally (e.g., by licking, sucking, biting, or chewing). Hypermetamorphosis referred to constant manual exploration and inappropriate attention to new stimuli, characterized by an immediate motor response upon the visual presentation of an object, regardless of its history or reward value. The term âhypermetamorphosisâ had been coined in 1859 by Breslau psychiatrist Heinrich Wilhelm Neumann (1814â1884), and then adopted and propounded by his assistant, German neuropsychiatrist Carl Wernicke (1848â1905), whose later monograph, Grundriss der Psychiatrie in klinischen Vorlesungen (Outline of Psychiatry in Clinical Lectures, 1906), conveyed the term and concept to KlĂźver [14]. Dietary changes of KBS included hyperphagia, pica, coprophagia, and ingestion of large quantities of meat (in normally vegetarian monkeys) [3, 5, 6]. Altered sexual behavior was manifest by a marked increase in the frequency and variety (i.e., autosexual, heterosexual, homosexual) of sexual activity, and also in a broadening of stimuli that would precipitate sexual excitation. What KlĂźver and Bucy initially called âpsychic blindnessâ and later sensory agnosia [1, 3] referred to the apparent inability to recognize and detect the meaning or significance of objects by sight in the absence of any evident impairment in visual acuity or ability. They found that some features of KBS (i.e., hyperorality,...