Developmental Vegetative State
Statement from Rays of Sunshine, the International Hydranencephaly Website and Support Group, regarding Consciousness in Congenitally Decorticate Children: "Developmental Vegetative State" as Self-Fulfilling Prophecy. The article was written by Dr Shewmon and published in Developmental Medicine and Child Neurology in June 1999. This article has brought hope to many of our families. Note: This article is quite long and technical. The reason for the technical language is that Dr Shewmon wrote this as a Neurologist for other Neurologists. He feels that is the way to affect change in the thinking of neurologists. If you don’t want to read all the technical stuff, read from “Why are these Cases so Rare” (p. 101) to the end."'
I have bookmarked this section for faster access “Why are these Cases so Rare” Ed., CHN
D. Alan Shewmon, MD
Gregory L. Holmes, MD
Paul A. Byrne, MD FAAP
in press, Developmental Medicine and
published June 1999
Address correspondence to Dr. Shewmon
UCLA Medical Center
P.O. Box 95 1752
Los Angeles. CA 90095-1752
According to traditional neurophysiologic theory. consciousness requires. neocortical functioning. and children born without cerebral hemispheres necessarily remain indefinitely in a developmental vegetative state. We report four children, ages 5 to 17 years. with congenital brain malformations involving total or nearly total absence of cerebral cortex, but who nonetheless possessed discriminative awareness. eg; distinguishing familiar from unfamiliar people and environments, social interaction. functional vision orienting. musical preference,, appropriate affective· responses. and
associative learning. These abilities may reflect "vertical". plasticity of brain-stem and diencephalic structures. The relative rarity of manifest consciousness in congenitally decorticate children could be due largely to an inherent tendency of the label "developmental vegetative state" to become a self-fulfilling prophecy
keywords: Congenital decorticate state; consciousness; developmental disability; hydranencephaly,: vegetative state
abbreviations AAN = American Academy of Neurology: CT = computed tomography: EEG=electroencephalogram. MRI=magnetic resonance imagine: PVS = persistent vegetative state
Content of consciousness is widely held to be mediated by the cerebral cortex, with subcortical structures serving merely an arousal function (Cranford 1988, Plum and Posner 1983). As the American Academy of Neurology (AAN) put it (1989):
"Neurologically, being awake but unaware is the result of a functioning brainstem and the total loss of cerebral cortical functioning... Pain and suffering are attributes of consciousness requiring cerebral cortical functioning.."
Equivalent statements have been issued by multiple professional groups (American Academy of Neurology 1995, American Medical Association 1990. ANA Committee 1993, Dyer 1992, Multi society Task Force 1994a. 1994b).
For congenital cases, the Medical Task Force on Anencephaly (l990) similarly opined: "Infants with anencephaly, lacking functioning cerebral cortex are permanently unconscious (p. 671).... the suffering associated with noxious stimuli (pain) is a cerebral interpretation of the stimuli; therefore, infants with anencephaly presumably cannot suffer (p. 672)"
According to the Multi-Society Task Force on persistent Vegetative State (PVS) (1994a. 1994b). any form of congenital decortication will equally yield a "developmental vegetative state" It takes but one counterexample to disprove a universal rule, We here present four.
PATIENTS AND METHODS
The following cases came to the authors' attention in a variety of ways. With full permission medical records were reviewed, and one or more authors visited the homes to examine the child and videotape interactive behaviors in the most familiar environment
Case I (VA)
VA was born full term following a pregnancy complicated by urinary tract infection. Hydranencephaly had been diagnosed prenatally by ultrasound. and parents relinquished the baby for adoption. His examination was unremarkable except for nystagmus and irritability.
Hydranencephaly was confirmed by computed tomography (CT). which showed absence of cerebral tissue rostral to the thalamus, save for small mesial temporal lobe remnants. A thin crescent of tissue extended from the left middle fossa along the posterolateral aspect of a large midline cyst with fluid of lower density than the main ruprafentorial fluid (Fig. I) EEGs showed no electrocerebral activity over the entire head except for some 50-60 pV theta plus low-amplitude beta in the left parietal region. corresponding to !he tissue on CT scan; some tracings also revealed epileptiform discharges in the same area.
VA was discharged to a foster family, who were told he would remain vegetative and almost certainly require institutionalization. Over the next two years he remained severely irritable and was treated with sedatives. By 6 months he had developed marked diffuse spasticity and prominent obligate tonic neck and grasp responses.
Hydrocephalus required placement of bilateral ventriculo-peritoneal shunts at age 4 months. The neurosurgeon observed no brain tissue at all under the meninges on either side. Increasing difficulty with swallowing led to placement of a feeding gastrostomy.
At 6 months VA was adopted by a nurse who had especially bonded with him and subsequently dedicated herself full-time to caring for three hydranencephalic children From then on he received constant stimulation and attention from both her and early-intervention therapists His neurologist from age 6 months to 10 years was author GLH.
When authors DAS and PAB visited VA at home. he was 6 years old He was small for age and microcephalic. extremely spastic with sustained clonus everywhere and moderate flexion contractures in all four limbs. He was well nourished and in excellent general heal health and was even mainstreamed in a normal nursery school. At age 10 he died unexpectedly for unknown reasons An autopsy was not performed.
Vision On examination at age 6 weeks he reacted to bright light: pupils constricted. but funduscopic examination revealed bilateral optic atrophy. Flash visual evoked potentials showed ''poor formation of the major positive component with a relative delay." On repeat at 6 and 25 months there was a retinal potential but no posterior waveforms. At 25 months a pediatric neuroophthalmologist confirmed the optic atrophy but noted that VA was attracted by light in the left eye's temporal field. there was nystagmus but "not really wandering vision of the blind." He concluded that VA had some vision and that only time would tell how much. At age 5 years, a neurosurgeon noted VA to be "fairly responsive to visual threat."
On examination by DAS at age 6, VA blinked to threat and closed his eyes to bright light. Although irregular conjugate nystagmus interfered with fixating, he grossly tracked objects and faces consistently and changes in affect or movement indicated active attending. His motor deficit precluded reaching for objects, but he visually interacted with the environment in other ways. such as scooting around the house (see below).
object discrimination. From age 3 on, therapists noted that he distinguished among toys, certain ones eliciting the most smiling. giggling, and moving. It is unclear whether there preferences were based on appearance, tactile quality, sound, or a combination thereof
Music Discrimination At age 6 weeks response to sound was documented. and auditory evoked responses were normal. At 3 years VA began regular music therapy. Therapists noted how he was consistently stimulated by music and reacted differently to different types of music. He distinguished new from familiar pieces and had clear favorites. While listening to Prokofiev's Peter and the Wolf during DAS's visit his behavior and facial expressions appropriately reflected the changing instrumentation and mood.
Goal directed behavior At age 2 the neuroophthalmologist documented that VA was fairly mobile when supine. pushing himself around in a circle with his legs. According to mother he could tell whether the sliding glass door to the sun porch was open and, if so, scoot through to enjoy the warmth and sunshine. Author PAB witnessed him scoot around the house. visually avoiding collision with walls and furniture.
Orientation. He would turn in the direction of someone calling him and smile.
Socialization. By age 3 VA's irritability had subsided. and positive affect became predominant. He smiled when spoken to and giggled when played with. These human interactions were much more intense than. and qualitatively different from, his positive reactions to favorite toys and music. He never developed stranger anxiety.
"Mirror test" During the authors'' visit, VA showed fascination with his own reflection. Despite efforts to distract him, he kept turning back to it, studying it intently and smiling.
Case 2 (DC)
DC was born full term following an unremarkable pregnancy and delivery Examination was normal except for a head circumference of 42 cm and widened sutures. Her entire; head transilluminated. Arteriography showed poor visualization of anterior and middle cerebral arteries but normal external carotid and vertebro-basilar systems (posterior cerebrals not specifically mentioned). During placement of a ventriculo-atrial shunt, the only subpial tissue found war a thin fibrous membrane. histiologically hemosiderin-laden and devoid of neurons.
Parents were told DC would remain vegetative and probably die within a few months. so she was institutionalized. Spastic quadriplegia and cortical blindness soon manifested At age I:1/2. still unresponsive. she was taken into foster care by the same nurse who adopted VA.
Hydranencephaly was reconfirmed around 51/2 years. when author GLH became her neurologist CT scan showed no supratentorial parenchyma above the thalamus, except for a thin left inferior temporo-occipital remnant and even less on the right (Fig 3). An EEG was isoelectric except for low-amplitude nondescript activity in the temporo-occipital regions.
She developed brief staring and longer tonic episodes, treated as seizures although of unclear nature. She ate orally until age 10, when tube feeding became necessary.
When examined by authors DAS and PAB at age I3. she had marked positional plagiocephaly, head circumference of 56 cm, and bilateral optic atrophy. Pupillary reflexes and extraocular muscles were intact, with wandering gaze and nystagmus. She had marked spastic quadriplegia with axial hypotonia and muscle wasting. She could move her right arm and kick with both legs. Emotion was manifested through facial expression and vocalization.
DC developed regular, brief menstrual periods around age 14- 1 5. transiently exacerbating her "seizures." She remained healthy until age 17, when increasing lethargy set in. Shunt malfunction was suspected, but hospitalization and invasive procedures were foregone. and she died peacefully at home. No autopsy was performed.
Although motorically and visually,· DC was much more disabled than her foster brother VA, she exhibited finer, though subtle, cognitive abilities.
Vision. Light/dark discrimination evidenced early. She had difficulty sleeping in the dark and "complained" until lights were turned back on. Around 4 years she began to track objects intermittently and became upset if her view was blocked. An optometrist found visual evoked responses to flash. gross checkerboard and bar gratings, suggesting acuity between 20/600 and 20/200. Waveforms were simple and at a markedly prolonged latency around 200 msec. Over the years. mother became convinced that DC sometimes identified her by purely· visual cues. About half the days DC seemed to see. The visit by DAS and PAB fell on a "bad" day: she rolled her eyes to bright light but showed no tracking or optokinetic nystagmus.
Discrimination of Persons. When received into foster care at age 1 1/2. DC showed no interaction with persons or environment. From then on she received constant affection and multimodal stimulation from her new mother and a therapist. For the next half year she remained unresponsive even to this enriched environment. Gradually, however, both mother and Iherapist noticed that she seemed more at ease in her own home than elsewhere.
By age 5 she consistently recognized certain individuals nonvisually and responded to people differentially according to three categories: mother, familiar persons. and strangers The more familiar someone was, the more she would relax, move spontaneously and vocalize. At age 6 a neurosurgeon described her as happy and very responsive to mother.
At age 12 her neurologist author GLH, noted that she smiled, turned to sound, and seemed to enjoy music. She was aware of mother's presence and became upset if separated. On author PAB`s first home visit, DC grew anxious at his approach and withdrew fearfully when he gently took hold of her arm, but calmed again to comforting by mother. During the joint visit of DAS and PAB. she seemed to enjoy being stroked by mother and was relaxed with a familiar music therapist: but when DAS approached. speaking soothingly and touching her as gently as possible, she became tense and apprehensive. with a change in respiratory pattern and more eye deviation toward mother at the other side of the bed
Musical discrimination Between 3 1/2 and 4 DC first manifested preference for certain kinds of music (ballad,, rhythmic dance. or marcher) and particular songs (eg. Send in the Clowns). as well as dislike for other kinds of music (Mozart, loud rock), From age 6 to I2 she was visited weekly by a particular music therapist, who eventually (after more than a )ear) was accepted into DC's circle of "familiar people", The therapist confirmed that DC was typically indifferent to most new pieces. but giggled and kicked to favorite pieces. If the therapist intentionally made an error or suddenly switched songs in the middle of a favorite one. DC would change facial expression turn head or eyes. and cease vocalizing. She preferred live music to recordings of the same pieces. and responded more to this therapist singing a favorite song than to an unfamiliar therapist singing the same song She would also orient toward, and reach out to touch. a nearby sound source.
DAS's visit coincided with a return of this therapist who had been away several months. The two quietly entered DC's room, and the therapist began to sing Send in the Clowns, accompanying herself on the piano. DC was at first expressionless but seemed to attend. After 45 second. she began to smile and gradually became more animated, with smiling, vocalizing and movement When DAS played the same version of Send in the Clowns, DC was less responsive. As mother predicted, she had no reaction to Mozart and romantic works, but became animated and vocalized to two bouncy dances from a Bach partita. She became indifferent again to slower movements from the same work.
Case 3 (OA)
Following an uneventful pregnancy OA was delivered by Cesarean section for breech presentation with birth weight 3.785 kg and head circumference 38 cm. Magnetic resonance imaging (MRI) revealed a gross brain malformation mainly resembling hydranencephaly but partially alobar holoprosencephaly. The Supratentorial space was empty except for a thin slab of frontal lobe a without midline fissure. A repeat scan at 10 months was unchanged.
Mother was told that OA would forever remain a "vegetable" and most likely not survive beyond 2 years. A neurologist, after reviewing the MRI, said that OA’s brain was "like that of a reptile" and that she would never socially interact. Her hydrocephalus steadily increased. but shunting was discouraged on the grounds that it would only lead to "more suffering.' on OA’s part. and institutional placement was urged. At age 2 months her feeding slowed to only 2 ouncer every 8 hours, and mother was told that OA's few brain cells were "dying." Despite such negative assessments, mother insisted that a ventriculo- peritoneal shunt be placed; if has since functioned well, requiring one revision at age 4 1/2 years.
At 6 months. OA was transferred to a new pediatrician and began "relaxation and distraction therapy." Soon her initial irritability subsided and the began to eat well She has remained in excellent health. An awake EEG at age 5 1/2 showed moderate-amplitude 2-5 Hz frequencies frontally, but no definite electrocerebral activity elsewhere amidst much artifact.
OA was 5 1/2 years old when visited by author DAS She had a happy. engaging affect. Head circumference was 51 1/2 cm. A hyperactive blink reflex did not habituate to glabellar tapping. though eye fluttering to a ratchety noise did. Cranial nerves were unremarkable. She had spastic quadripareris. sustained clonus, palmar and plantar grasp reflexes, and bilateral Babinski signs. Despite axial hypotonia she could raise her head and control it somewhat when propped sitting. A stepping reflex enabled her to "walk" with axillary support.
Vision: After only a few weeks mother suspected that OA could see. Between 4 and 5 months she began to smile responsively, and thereafter vision was unquestionable. She was evaluated twice around age 2 by an ophthalmologist, who noted that fundi uere normal and visual fixation was -'central. steady and maintained." Acuify was not estimated. For DAS she demonstrated a nonhabituating "virtual suck" reflex, in which her mouth would open and tongue protrude at the approach of any object. She smiled responsively, tracked faces and toys, and oriented immediately to objects brought into the visual periphery.
Orientation. When called, she would raise her head, look at the person and smile
0bject Permanence. When an object she was tracking while held sitting was suddenly whisked behind her, the would turn in search of it.
Person discrimination Between 3 and 4 months the manifested a slight preference for mother She never developed stranger anxiety, but senses if someone is uncomfortable with her and stiffens. She cried constantly during a visit of a therapist whom mother described as "condescending" As soon as the therapist left, she stopped crying and smiled at mother. She developed a liking for puppies and small children: her eyes "light up" whenever the sees one.
Socialization She clearly enjoys being with people and even interactively plays. A "conversation" with mother is documented on video. in which OA attempted to imitate monosyllables and even uttered "ah-ah" to coaxing to say "mama." In another scene she attempted to stick out her tongue in an, imitative game with mother, finally succeeding
Musical and emotional discrimination. By history. when OA hears a happy song she enlivenrs and seems to want more when it ends; conversely, she tends to cry with sad songs. During DAS's visit she did enjoy some happy songs, but no sad songs were available for comparison. Once when a babysitter was crying. OA began to cry sympathetically.
Body awareness. At 6 months OA began to manifest awareness of her body. eg. if her face was hurt, she would stroke it with her hand. She enjoys vestibular and vibratory stimuli: eg.. during a car ride, she cried at stop and immediately calmed upon resumption of motion.
Associative learning. She startled and stiffened when a vacuum cleaner or hair dryer war turned on. making a loud unpleasant noise. After several such experiences, she also stiffened in anticipation if either object (though .'off') was brought near. She developed a small receptive vocabulary)·. including "bunny rabbit" (a stuffed toy), "Michael" (a family friend), and Pocahontas" (an image on her T-shirt): with coaxing and repetition of the question. "Where is [one of these". she correctly looked at the object or person.
Case 4 (RB)
RB was born to a single mother who intended adoption. Because of abnormally positioned ears a CT scan was obtained, diagnosing hydranencephaly. On re-examination his head transilluminated. RB was adopted at 6 weeks by a former nurse who provided a home for disabled children, She was told that he would die soon and never develop relatedness..
RB soon demonstrated severe spastic quadriplegia. Despite physical therapy, diazepam, and baclofen marked flexion contractures developed. He required gavage feeding for two years, but then ate orally until age I I, when a gastrostomy tube had to be placed.
RB has always appeared cortically blind, with some response to darkness and light but no visual tracking. An ophthalmologic examination revealed severe optic atrophy.
Seizures were suspected, with motionless staring, often progressing to head deviation and facial twitching for around a minute, followed by drooling. Phenobarbital was begun and is still taken: seizure frequency is now around two per month. Three EEGs, at ages 4,. 4 1/2 and 9 1/2 years. all showed no activity in frontal, central and temporal leads. The occipital region had frequent epileptiform discharges and no change with eye opening or closing.
At age 10. RB required a permanent tracheostomy for airway obstruction due to macroglossia. A CT scan at that time showed occipital lobe remnants but no other cerebral cortex. Posterior fossa structures were normal. Since then, he has remained in excellent general health, puberty began around 13 or 14 years.
At ages 9. 12, 14 and 17, RB was evaluated with the Vineland Adaptive Behavior Scales, Age-equivalent scores ranged initially from 4 to 10 months and recently from I to 5 months. with a decrease in the Daily Living domain related to inability to take food orally.
He was 17 years old when visited by author DAS. Head circumference was 17 cm Pupils reacted to light. Eye movements were roving and nystagmoid, without fixation or following Extremities had fixed contractures. and reflexes were hyperactive with sustained clonus. Facial expression and slight head turning were his only means of communication.
Nonverbal communication and affect .At age 9 a developmental psychologist observed cooing sounds, expressions of sadness or pain, and smiling in the presence of caregivers. At age 14. on re-evaluation he cooed and laughed. and by age 17 he indicated preferences through facial expressions and a broad smile.
Person recognition. Ability to distinguish mother became evident around 2 years. when he would stop sucking a bottle and attend when mother spoke to him but not when others; did. Ever since he has reacted indifferently to strangers but positively to her. His eyes often turn toward her voice. even though he does not see. When at age 10 he was taken to the hospital for upper airway) obstruction. she had to accompany him in the ambulance: as long as he heard her reassuring voice and felt her caresses his oxygen saturation remained tenuously stable, but whenever the stopped. it quickly deteriorated
This discriminative ability was repeatedly corroborated by the developmental psychologist,. who noted that at age 9 RB smiled in response to caregivers, at 12 and 14 he distinguished mother's from father's voice, and at 17 he enjoyed mother stroking his face and tolerated pain better in her presence. During DAS`s visit he was unresponsive to the author's attempts at vocal and tactile interaction. but smiled consistently to mother's voice and touch.
Orientation. At ages 9 and I2 he was documented to turn head and eyes toward sound and his head toward tactile stimulation.
Musical discrimination RB`s mother frequently exposed him to music. At age 14 the psychologist noted that he enjoyed music, particularly with deep sonorities. From 16 on. he has had weekly sessions with a music therapist. She gradually found that particular pieces and types of music (eg. with strong rhythms and high-pitched instruments) elicit positive affect more consistently than others: he smiles radiantly and sometimes laughs. whereas his affect blunts when the music stops or less favorite pieces are played. Environmental sounds elicit no such response. He distinguishes live instruments and especially enjoys the therapist`s maracas and tambourine and to hare the stereo speaker placed on his chest. At times he has followed the sound of her maracas with his eyes as she walked around his bed
During DAS`s visit the music therapist came, and these differential responses were observed. when DAS played some classical music RB remained apathetic, but he smiled and became animated with a tape of "Favorite" band music accompanied by live maracas.
Each of these children defied a prognosis of permanent vegetative state, rendered with absolute certainty by multiple physicians, including pediatric neurologists and neurosurgeons. Any one of these cases suffices to disprove that all content of consciousness, including pain and suffering. is necessarily mediated by the cortex. That four such cases have come to the authors' attention through pure happenstance suggests that subcortical mediation of consciousness in congenitally decorticate children might not be so uncommon as the Multi-Society Task force seeml to imply (1994a (p 1504) These findings therefore raise important questions about our assumptions regarding consciousness and brain plasticity.
Is the cortex necessary for consciousness?
It would far exceed the present scope to enter into a philosophical discussion of the definition and possible operational criteria for something so fundamental yet elusive as "consciousness." Suffice it to emphasize the term's inherent ambiguity. deriving from the `'bidimensionality" of human consciousness; the simultaneous awareness of the physical world (including one's own body) and awareness of that awareness (i.e.. "self-awareness. "reflective awareness") (Plum and Posner 1983 (p1).
The AAN position statement on PVS (1989) implicitly ascribes to "consciousness" both dimensions paraphrasing "eyes-open unconsciousness" as a state in which "at no time is the patient aware of him,- herself or the environment" (emphasis added). Similarly, its more recent "practice parameter" defines "vegetative state" as involving "complete unawareness of the self and the environment" (emphasis added) (American Academy of Neurology 1995), Nevertheless. biologists (not to mention animal rights activists) speak meaningfully of "consciousness" in animals where only the behavioral. operationally definable, non-reflective "dimension".. is implied. Unarguably. such "consciousness" is just as properly attributed to the decorticate children described here. Were they not humans studied by clinicians but rather animals studied by ethologists, no one would object to attributing to them "consciousness" (or ability to "'experience" pain or suffering) based on their evident adaptive interaction with the environment This alone is surely remarkable. Even prescinding from the question of self-awareness. the possession by decorticate children of even animal-type "consciousness'· thoroughly contradicts prevailing PVS orthodoxy, which predicts that they should be precisely vegetative, not sentient and intentionally behaving.
Whether or not their consciousness also has an ··orthogonal" reflexive dimension is empirically unanswerable. Self awareness cannot be reduced to mere external manifestations (ie e. linguistic self-reference): neither can its absence be inferred from mere absence of such manifestations. especially if the linguistic apparatus is pathologically or developmentally inadequate. Far example. there is no reason to suspect that autistic children. global aphasics. and preverbal infants lack reflective awareness merely because they do not talk about it.
Some authors claim that the best test for self-awareness in animals is recognition of their own body in a minor (Korein 1997). Whether behavior before a mirror reflects true self-awareness of a mind. as opposed to an extension of body-awareness or even mere fascination with control over the image's movements (perceived as extra-self). is debatable. In any case. VA was as interested in his reflection as any infant or simian who passes the "mirror test.'
Although agnosticism about self-awareness might theoretically be the only scientifically rigorous position, practical prudence demands giving the benefit of the doubt
that any member of the species Homo sapiens who is behaviorally conscious is reflectively so as well. Thus have we always treated autistics and aphasics. Only recently, however, has the same enlightened stance been extended to preverbal infants (Anand and Hickey 1987), and there is no a priori reason not to extend it also in decorticate children with environmental awareness. After all. we feel compelled to treat "humanely" laboratory animals with even smaller brains.
Were these children truly decorticate?
One might argue that the remarkableness of these cases is muted by the fact that none of the children was absolutely devoid of cortical tissue: they were not truly· "decorticate"·
The proper nomenclature for VA's and OA’s pathology is admittedly debatable: it is more dysgenetic than classical hydranencephaly (the end-product of in utrero necrosis of normally developing hemispheres (Halsey et al 1971, Samar 1992)). VA had mesial temporal remnants and a large supratentorial cyst partially lined by tissue capable of generating epileptiform discharges OA has a sliver of holoprosencephalic frontal lobe. But the point is. even if these two children were not "decorticate' absolutely. they were enough so that physicians. including neurologists. predicted a vegetative outcome absolutely
Even in classical hydranencephaly there is often a thin remnant of inferior temporo- occipital cortex. (Halsey et al. 1971), as exemplified in cases DC and RB. Typically this tissue does not mediate vision because it is severely gliotic and optic radiations are absent. Thus. despite the cortical remnant. such children are universally cortically blind, as was RB (and DC on "bad" days). and the literature does not hesitate to label them "decorticate.. (Berntson et al 1983. Deiker and Bruno 1976. Halsey et al 1968) and to consider them as necessarily vegetative (Multi-Society Task Force an PVS 1994a (p 1504))
The most important differential diagnosis is with "maximal hydrocephalus." in which the cortex is basically intact though extremely compressed (Linuma et al 1989. Sutton et al 1980) Refinements of modern neuroimaging make this distinction less difficult than it used to be Also. the EEG is relatively normal in maximal hydrocephalus but virtually flat in hydranencephaly. In each of our four cares all diagnostic information taken together leaves little ground for concern over possible misdiagnosis of maximal hydrocephalus.
The main point is that these children's consciousness can be inferred to be mediated subcortically not, because there were absolutely zero cortical neurons, but because the few that were present could not plausibly subserve the totality of their conscious behaviors. That is why parents were invariably told -with complete confidence by relevant specialists - that their child would unquestionably remain in a vegetative state for as long as he or she lived. Experienced neurologists, to whom the authors have shown the CT and MRI scans with an invitation to guess the child's Ievel of functioning. also typically predict vegetative state.
This is not to say that the number and distribution of telencephalic neurons played no role in these children's cognitive repertoire. The two with rudimentary limbic structures (VA and OA) were more affective and sociable than the two with classical hydranencephaly·. and they also had more motor function. Ironically, they also possessed the most vision despite total lack oloccipital cortex. in contrast to the other two, who had little or no vision despite occipital remnants. It seems as unlikely that the occipital tissue in the latter two mediated their discriminative affect as that the limbic tissue in the former two mediated their vision. What is functionally common to all (consciousness per se) is more logically attributable to structures common to all (diencephalon and brain stem) than to idiosyncratic structures (OA's frontal sliver, VA's mesial temporal tissue, and DC's and RB’s occipital slabs,)
In principle the anatomical substrate of their various cognitive functions could be clarified noninvasively by high-resolution positron emission tomography. or less practically by· functional MRI Unfortunately. logistical and economic obstacles precluded such tests. and we must make do with inferences from the information available
Do subcortical structures possess "vertical" plasticity?
That subcortical mediation of consciousness has been described so far only in congenital brain malformations suggest that developmental plasticity may play a role. Although both cortical plasticity for cortical functions and subcortical plasticity for subcortical functions ("horizontal" plasticity) have been known for many decades (Cotman 1985, Finger and Wolf 1988. Flohr and Precht 1981), subcortical plasticity for supposedly cortical functions ("vertical" plasticity) has not previously been reported. apart from cases VA and DC in an abstract (Shewmon and Holmer 1990) and mentioned briefly elsewhere (Shewmon 1992).
Vertical plasticity must be less robust than horizontal plasticity: intuitively, potential for compensatory reorganization ought to be largely related to the degree of microstructural similarity between sites at issue. But it would be gratuitous to exclude a priori the very possibility of vertical plasticity. Perhaps the strongest argument for its role in our cases is that the two children with vision despite fetal absence of occipital cortex had brain malformations arising earlier in gestation than the two with no vision despite occipital remnants. presumably in the latter cases, prior to telencephalic infarction the visual system had developed so that relevant subcortical nuclei were already committed to a functional relationship with occipital cortex whereas in the former the absence of occipital cortex all along allowed these subcortical nuclei "free rein'· to organize optimally for functional vision.
If such vertical plasticity can occur with vision there is no reason to suppose it cannot also occur to some extent with other sensory and motor modalities and with their mutual interactions mediating adaptive environmental relatedness. i.e. with consciousness (at least its behavioral. operationally definable dimension). This should not be surprising, given:
(I) the primarily subcortical mediation of certain sensory modalities. especially pain
(Bromm and Desmedt 1995, Lenz 1991, McQuillen 1991, Willis 1989) with cortex serving a more modulatory role (Talbot et al 1991)
(2) the non-postulation of any cortical representation certain other sensations. especially visceral ones such as nausea, thirst, etc. (Brookhart et al 1984, Kandel et al 1991)
(3) the distinction between pyramidal and extrapyramidial motor systems,. the former governing fine distal activity and the latter gross, proximal/axial activity (Davidoff 1990, Lawrence and Kuypers 1968a, 1968b, Sarnat 1989) (with hemispherectomy loss of individual finger movement is a pyramidal deficit, whereas gait and use of the paretic arm as a "helper" derive from the extrapyramidal system: our cases are motorically and anatomically equivalent to bilateral hemispherectomy)
(4) the role of the nucleus reticularis thalami in attentional focus and relevance-based pre-cortical sensory "filtering" Crick 1984, Hobson and Steriade 1986, Scheibel 1984) and
(5) the "distributedness" (both horizontal and vertical) of brain systems mediating higher functions (Freeman 1990, John 1990, Mesulam 1990, Pribam 1990)
The hydranencephaly literature documents subcortical mediation of certain cognitive functions usually attributed cortex, such as distinguishing mother, associative learning. consolability. conditioning, orienting, and visual tracking (Aylward et al 1978. Barnet et al 1966. Bemlron and Micco1976, Berntron et al. 1983, Brackbill 1971, Deiker and Bruno 1976. Francis et al 1984. Graham et al 1978, Hairy et al. 1968, Nielsen and Sedgwick 1949. Tuber et al 1980).
In the pre-CT scan era Lorber (1965) described a remarkable case of a boy diagnosed with "hydranencephaly" by pneumoencephalogram who had developed normally as of 21 months of age. The X-ray seemed to show air right up against the inner table of the skull. Nevertheless normal development is so implausible with hydranencephaly yet perfectly in keeping with maximul hydrocephalus that one cannot help doubting the sensitivity of the air study. Lorber seated that an EEG -showed evidence of some electrical activity." but its quality and distribution were not described. If the EEG was as relatively normal as the child, then surely this was misdiagnosed hydrocephalus. Lorber concluded. "there ought to be some cerebrum somewhere, as it is impossible to explain his progress otherwise At this stage. one can go no further and he remains... an enigma." fifteen years later. Lorber reported patients with cortex as.thin as I mm from hydrocephalus, yet neurologically normal (Lewin 1980) Follow-up on the normally developing 'hydranencephalic" boy, however, was not provided.
The cases reported are not at all similar to Lorber's; they had gross brain dysgenesis or bona fide hydranencephaly, and all were cognitively and motorically severely disabled The impossibility of their having misdiagnosed maximal hydrocephalus reinforces more convincingly Lorber's and others speculation that subcortical structures may play a greater role in consciousness than is usually assumed (Berntson and Micco 1976, Lewin 1980).
Some authors have hypothesized primarily subcortical vision in normal human newborns prior to postnatal encephalization (Bronson 1974, Snyder et al 1990) Fetuses in utero can distinguish and remember sounds (DeCasper and Spence 1986, Restak 1986) and term infants prefer mother's voice to other women's. and women's voices to men's (DeCasper 1980), even though they have very low cerebral cortical metabolism not dissimilar to adults diagnosed in PVS (Chugani et al 1987. Levy et al 1987)
There is also phylogenetic precedent for subcortical mediation of some complex behaviors and perceptual functions traditionally regarded as'` cortical." Eg.. habituation. learning. and discriminative conditioning have been observed in decorticate animals (Bromiley 1948. Finger and Stein 1982 (pp 245-250), Huston and Borbely 1974, Norman et al 1977, Travis and Woolsey 1956). Binocular depth perception is exhibited exquisitely by falcons. owls, toads and grass frogs, although they possess little or no visual cortex (Collet and Harkens 198t. Fox et al 1997, Pettigrew and Konishi 1976). and it can be brought out in cats following bilateral occipital lobectomy (Feeney and Hovda 1985. Hovda et al 1989. Hovda and Villablanca 1990). Feline vertical plasticity is evidenced in that adult cats bilaterally hemispherectomized as kittens behave nearly indistinguishably from normal. in marked contrast to cats hemispherectomized as adults (which are severely disabled) (Bjursten et al 1976. Burgess and Villablanca 1986. Burgess et al 1986. Villablanca et al 1986)
This animal evidence is cited, not to imply that cortex and subcortical structures must have the same role in humans as in animals and the same potential for plasticity (the perils of cross-species extrapolations are well known), but rather to emphasize how much more parsimonious it seems (absent direct data) tentatively to ascribe OA's visual function, for example, to subcortical pathways known to subserve vision in animals rather than to her rudimentary frontal lobe: much less radical reorganization would have to take place. On the other hand, the cortex's capacity for transmodal reorganization may also be greater than previously imagined, as evidenced by recent studies of occipital activation by tactile Braille reading in people blind from an early age (Büchel et al 1998. Cohen et al 1997). Clearly this exciting field is wide open for fruitful research.
Why are such
cases so rare?
But if consciousness in congenitally decorticate children occurs by virtue of diencephalic and brains stem plasticity. why should it not occur in all, or even most. such children? Five possible reasons suggest themselves.
1. Susceptibility to unfamiliarity First decorticate children are extremely sensitive to changes in routine and environment. They are easily disturbed by rides to doctors' offices and by strange people and surroundings, in such settings they often involute and fail to manifest any cognitive functions that parents might report. (This is why home visits or home videos are a particularly important means of documentation.)
2. Intermittence of function Secondly, certain functions may be intermittent even at home (eg; VA's scooting, DC's tracking), reducing still further their probability of being witnessed during a brief office visit. let alone in an emergency room or intensive care unit
3. Physicians' lack of time. Thirdly, the preceding two obstacles are compounded by the brevity of time that doctors often have for taking detailed developmental histories and examining for subtle functions that may not be immediately manifest.
4. Mental filtering Fourthly we physicians have learned through experience to interpret implausible parental claims about abilities of severely disabled children as psychological denial. On the other hand, we should be on guard against a form of denial ourselves, ignoring evidence inconsistent with our (often simplistic) theories of brain functioning. We all probably engage in more selective information-filtering than we would like to admit.
5. Self-fulfilling prophecy But perhaps the most important reason why such cases are so rare is that the label "developmental vegetative state" tends to be self-fulfilling. Sensorimotor and emotional deprivation in even neurologically normal infants leads to profound apathy, failure to thrive and developmental delay (Dietrich et al. 1983, Koluchova 1972. Money 1977. Perry et al 199S. Powell and Bettes 1992. Weston et al 1993). How much more should such consequences be expected if the deprived infant is severely disabled. Nevertheless, the uniformity of "vegetative" outcomes in decorticate infants treated as ”vegetables" is accepted uncritically by many as "evidence" that congenital decortication necessarily produces a "developmental vegetative state".` This is analogous to the now acknowledged tragedy of many potentially functional individuals with Down syndrome who became victims of self-fulfilling prognoses of severe mental retardation (Canning 1978. Zausmer 1978).
Indeed, the parents of all four children reported here were initially warned by most physicians that their child would unquestionably never have a mental life. Whether some physicians actually used perjorative terminology, or parents simply reinterpreted over time the recollection of those conversations, matters little for understanding the self-fulfilling tendency of the label "developmental vegetative state.'. Regardless of the words spoken. parents were often left with a sense o of not merely a bleak developmental outlook but even a dehumanizing attitude toward the child. On occasion (eg. when the child was brought to an emergency room or required intensive care) some parents were given the impression that certain physicians felt they were wasting valuable time and "scarce resources" on something subhuman or even sub-animal (i.e, a "vegetable." even if the word was not used explicitly)
If these children had been kept in institutions (as DC was for the first 1 1/2 years) or treated at home as "vegetables" (the prognosis being accepted uncritically by parents). there can be little doubt that they would have turned out exactly as predicted· What surely made all the difference was that their parents ignored the prognoses and advice, and instead followed their instinct to shower the children with loving stimulation and affection. Such children and their families have much to teach about not only the neurophysiology of consciousness.
The authors wish to thank Mr. Stephen Wire for assistance in the photography
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