Twenty years ago,1 we considered the effects of brain injury on various disorders of the nervous system, such as multiple sclerosis, syringomyelia and neuritis. We also touched briefly on behavioral effects of trauma, mostly in relation to classical psychiatric diagnoses. Today the effects of trauma on these and other nontraumatic syndromes seem less important, though still occasionally relevant as ancillary etiologies. In contrast, direct effects of nervous system trauma have assumed great medical importance with the modern epidemic of head injuries resulting from motor vehicle accidents and accidents of other types. This article will be concerned with advances of knowledge published over the past two décades derived from studies of large numbers of accident victims and victims of war injuries. We will limit our attention to the present state of understanding of direct behavioral effects of head injuries in adults.
Both improved transport with shortened delay between injury and definitive treatment, and increased knowledge of pathologic mechanisms have improved chances for survival of patients with severe head injuries. Training of ambulance personnel in the importance of gentle and expeditious handling to avoid spinal cord injury, care for maintenance of respiration, and other modern techniques of emergency care have all helped. Finally, improvements in diagnosis and definitive treatment of the effects of nervous system trauma have enabled the neurosurgeon to save individuals who would have died in the past. Survival has become more likely, but the brain damage leaves many of the survivors with significant neurologic or behavioral deficits. The improvement in care has paradoxically resulted in a considerable increase in the number of head-injured patients with post-traumatic deficits in intellectual and social function.
A report by the National Head and Spinal Cord Injury Survey,2 has estimated that 926,000 head injured individuals hospitalized between 1970 and 1974 still exhibited sequelae in 1974. This figure does not include the estimated 50% of patients who died before arrival at a hospital3 or patients who were injured before 1970 and were still hospitalized. Annegers and Kurland4 estimated that in 1975 there were 663,000 head injuries more severe than "concussions" in the US. They also suggested that an equal number of minor head injuries were unreported.
Thus the present review necessarily will be limited to a select group of head injured patients, those who have reached the hospital alive and have thereupon been hospitalized and studied.
TYPES OF LESIONS
Brain lesions of head injury are ordinarily reported as focal or diffuse. Focal lesions cause specific neurologic deficits, as demonstrated by thousands of informative clinical studies over the years. The term diffuse brain injury can be misleading when used to suggest some sort of mass functional disturbance. Diffuse brain injury more realistically consists of a complex of multiple focal lesions. The modern view was summarized by Newcombe5 in his report on the psychological effects of missile wounds of the brain, where he concluded that "these findings do not lend any support to a mass-action theory of brain damage.
Figure 1. The Glasgow Coma Scale.
In recent years, computed tomography has provided graphic confirmation that diffuse brain injury consists of multiple focal lesions, with the demonstration following severe head trauma of tiny punctate hemorrhages scattered throughout the parenchyma.6 At times these hemorrhages are so numerous as to assume a "pepper and salt" pattern on the CT scan. Such parenchymatous lesions often appear to result from shearing forces at junctions between soft masses of gray matter and adjacent firmer masses of white matter. Associated with and accounting for these scattered punctate hemorrhages are multiple ruptures of small blood vessels and nerve fibers - presaging a serious prognosis.
Commonly the clinical effects of such multiple lesions appear generalized, as demonstrated by diffuse EEG changes and metabolic alterations. It has become clear that the actual lesions indeed are not generalized, occurring only at the local sites where traumatic shearing forces concentrate.
EARLY EVALUATION OF HEAD INJURIES
The early evaluation of patients with head injuries has received much attention. Quantification of clinical state has been shown to be very important, both for immediate neurosurgical or medical therapy, and as a key to ultimate prognosis. The best known of the quantitative protocols for the evaluation of head injuries is the Glasgow Coma Scale7 (Figure 1).
Figure 2. Galveston Orientation and Amnesia Test (GOAT).
Because the Glasgow Coma Scale quantitates only the level of consciousness, other scales have been devised to evaluate functional deficits apparent after recovery from coma. The brief questionnaire developed by Levin, O'Donnell and Grossman,8 the "Galveston Orientation and Amnesia Test" (GOAT) is applicable when the patient recovers the ability to converse more or less coherently, and thus covers a period not included in the Glasgow Scale (Figure 2).
Several other scales have been devised. For example, investigators at Albany Medical College9 have devised an elaboration of the Glasgow Coma Scale, giving a fuller view of the patient's abilities and disabilities.
Figure 3. Temporal relationship between injury, coma, and periods of amnesia.
OUTCOME AND FUNCTIONAL RECOVERY
The Glasgow Coma Scale has been known long enough for investigators to make use of it in statistical evaluation of patient outcomes. For instance, Heiden et al10 correlated the Glasgow Coma Scale at 24 hours post-injury with the one-year outcome. Of those most severely injured, with scores of 3 or 4, only 5% had good recovery at one year; if the 24hour score was 8 or more, 83% did well.
Age has a strong effect on the eventual outcome after severe head injury. Heiden et al10 reported that of 24 patients over 60 years of age, all were either dead or in a persistent vegetative state one year after injury. Of 39 patients aged less than 20 years, on the other hand, 62% made good recoveries.
Amnesia stands out as the single most common disturbance of higher level function associated with head injuries of any degree of severity. Russell's monograph of 1971 " summarizes most of the modern ideas on traumatic amnesia. Amnesia for events prior to the injury, retrograde amnesia, ordinarily has a much shorter duration than amnesia following the injury, post-traumatic or anterograde amnesia. Figure 3 graphs the time sequence of amnesia related to a head injury.
In contrast to the pattern suggested by Figure 3, amnesia may be discontinuous, particularly with severe head injuries. There may be "islands" of retained memory in the midst of periods of retrograde or post-traumatic amnesia. Difficulties may arise in ascertaining duration of amnesia because of these islands, and because complex acts may be carried out during amnesic periods. Following minor head trauma, football players have been known to Carry through complex plays for which they later have no memory.
Russell describes a common sequence of posttraumatic recovery of speech, social functions and memory. n At first the patient is unable to produce any words, and groans and shouts continuously. Next he meaninglessly repeats a few words, then Common phrases, with increasing vocabulary but without evidence of understanding. Incessant talk unrelated to anything said to him is followed by impudent and overly familiar comments to attendants. Eventually, insight, orientation and normal social habits follow as the patient begins to retain immediate memory, becomes aware that he has had an accident, and starts to think about events preceding and following his accident. (Parenthetically, the masculine pronoun is used here because male head injury patients outnumber females four to one.)
Durations of retrograde and of post-traumatic amnesia roughly parallel the severity of the injury, but no dependable relationship has been demonstrated. Patients beyond the age of 60 years are likely to suffer longer periods of amnesia. A 65year-old patient described by Levin, Benton and Grossman exemplifies this.12 She was struck on the head and was unconscious only a few minutes, but experienced disorientation, confusion and posttraumatic amnesia for 12 days. Jennett reported that 90% of patients with post-traumatic amnesia less than 7 days in duration had good recoveries, but if the amnesia lasted 28 days or longer, only 11% eventually did well.13
Even after the periods of global amnesia have ended, head injured patients often demonstrate residual memory deficits. Russell1 ' reported a 23% incidence of post-amnesic memory problems among a population of 1,324 World War II soldiers with closed head injuries. Those with longer periods of post-traumatic amnesia were most likely to have permanent residual memory defects.
It is interesting that forward (direct) digit span as a test of immediate memory does not accurately reflect the severity of memory loss in head injury. Similarly, other patients with lesions causing severe generalized memory defects, such as temporal Iobal herpes, bilateral removal of temporal lobes, or Wernicke-Korsakoff disease, often demonstrate normal or nearly normal forward digit span. On the other hand, reverse digit span is affected more often in these patients'4 as are more complex tests of memory. An illustrative example is the Selective Reminding Test of Buschke and FuId15 where 12 common words are presented verbally, to be repeated by the patient. On successive trials the examiner presents again only the words which were missed on the preceding trial. Most normal individuals reproduce the entire list correctly after about six trials, and women do somewhat better than men. An interesting side effect of injury shows up in head injured patients, after recovery from disorientation and in the absence of aphasie difficulties. Patients with pure right-sided lesions perform just within the normal range, while those with left-sided lesions, bilateral lesions or diffuse head injuries do very poorly.
In contrast to the deficits in verbal memory with left-sided lesions, visual memory usually suffers much more severely with right-sided lesions. Such patients often have great difficulty recalling geometric forms that have been previously presented.16 Recall of photographs of faces can similarly be deficient.17 As with amnesia, age exacerbates long-term memory problems following head injury.18
Though not proved, there exists much circumstantial evidence that damage to the hippocampus and adjacent portions of the temporal cortex may account for these disturbances of memory function.
GENERAL INTELLECTUAL FUNCTION
Levels of intelligence, defined as the numerical results of intelligence tests such as the Wechsler Adult Intelligence Scale (WAIS), its sub-sections, or similar tests of intellectual performance have been evaluated after head injury by a number of groups. Most observers have reported intellectual deficits in the immediate post-confusional and post-amnesic periods generally related to the severity of the injury. Long-term prognosis for recovery of intellectual function again roughly parallels the level of general recovery. In particular, patients do poorly if the injury produced brain stem signs such as pupillary or oculo-vestibular abnormalities.
Tests of verbal performance often show poor results when the major lesions are left-sided, while little effect may be manifested on the performance scales of the intelligence tests. Performance IQ often correlates better with the overall long-term outcome. Many more detailed statistica! studies will be necessary to clarify the specific effects of head injury on the various components of intellectual function.
Post-traumatic speechlessness, probably on the basis of aphasia, was mentioned in the Ebers Papyrus of ancient Egypt. Modern studies have generally emphasized the focal nature of causative lesions, and much has been learned about areas of the brain devoted to speech functions. Only recently have careful studies considered the effects of severe head injuries on speech.
Najenson et al19 plotted curves of recovery of language function over 18 months in 15 patients with prolonged coma. They observed a consistent sequence of recovery of communicative skills. Comprehension of gesture and of speech appeared first, within 3 to 20 months after severe trauma. The patient's speech, reading and writing were slower, and motor deficits of speech were last to recover, or often (8 of the 15) were permanent. Recovery of walking and of speech generally corresponded. Because evaluation of speech in the presence of confusion can lead to erroneous conclusions* proper evaluation of language requires concurrent measurement of orientation. Mild aphasia due to focal dysfunction in the immediate post-traumatic period can also be misinterpreted as a disorder of language associated with the more widespread injury.
Sarno examined 56 patients with severe closed head injuries, dividing them on the basis of clinical examination into 18 aphasies, 21 with dysarthria and subclinical language disorders, and 17 with "subclinical aphasia."20 The latter were identified by abnormal scores on the quantitative examination for aphasia devised by Spreen and Benton,21 but without obvious aphasia in conversational speech.
OTHER TYPES OF SPEECH DISORDER
Mutism, the total abolition of speech, commonly occurs between the first eye-opening and recovery of orientation. Long-lasting lack of speech (akinetic mutism, locked-in syndrome, or aphasie mutism) indicates severe injury. Akinetic mutism includes apparent wakefulness, normal sleep-wake rhythms, but no expressed relationship to the environment. The locked-in syndrome occurs in quadriplegic patients with facial paralysis but retained eye movements, and with retained consciousness. The lesion usually transects the pons, including both motor and sensory long tracts. With aphasie mutism the patient will exhibit other problems with language; dysgraphia, dyslexia, etc.
Echolalia, the repetition of words spoken by others, and palilalia, automatic repetition of one's own words, may occur as transient stages in recovery from head injury, or may be part of the Jongerlasting aphasie syndrome.
Dysarthrias represent the results of damage to the central or peripheral speech apparatus itself, and vary from minor problems with articulation, phonation and intonation to completely unintelligible speech.
Severe head injuries commonly involve the corpus callosum. Small hemorrhages in the corpus callosum as demonstrated by the CT scan presage a grave prognosis.6·22 Damage to the corpus callosum may lead to syndromes of hemispheric disconnection in head-injured patients as acute manifestations or long-term defects. Levin et al23 tested interhemispheric transfer of information by asking the patient to name objects placed in the right or left hand. Many patients had more difficulty naming objects placed in the left than the right hand, a finding interpreted as indicating callosal lesions.
Specific lesions of the visual system or of other sensory pathways cause specific sensory deficits. Decreased ability to recognize visual objects including familiar faces (prosopagnosia) often occurs during the early post-traumatic period in head-injured patients. Such reports have mostly been anecdotal, but suggest that this and similar visual problems might warrant careful investigation.
Tachistoscopic evaluation of visual perception has recently been reported24 in 51 patients, a year or so after closed head injuries of variable severity. The expected correlation was found between severity of injury, as determined by duration of coma, and the tachistoscopic time required for recognition of sequences of three letters. Interestingly, no difference was found between right and left visual fields. These patients were not confused at the time of examination, and had no visual field defects.
Reaction times showed a similar corrélation with severity of head injury in a study of 57 young men with post-traumatic coma, defined as a score of 8 or less on the Glasgow Scale.25 Patients with coma lasting less than one hour had the fastest reaction times, followed by a second group with coma between 1 hour and 7 days, and the slowest was the group with coma lasting more than 7 days. Simple reaction times improved slightly over 24 months. Improvement was considerably more obvious and statistically significant with multiple-choice reaction times.
PSYCHIATRIC SEQUELAE OFHEAD INJURY
Head-injured patients may demonstrate posttraumatic confusion, hallucinations, paranoid ideation, depression, and confabulation. Confabulation during the acute post-traumatic confusional state probably occurs in a large percentage of head-injured patients, but definite statistics have not been collated. Blatant psychosis, manifested by bizarre behavior, probably has an incidence of only a few percent among unselected head-injury patients. Schizophrenia-like illness following head injury generally does not include organized delusional systems of the types seen in schizophrenia. The delusions tend to be fragmented and disorganized. Paranoid ideation commonly relates to delusions of body harm.
Concussion is defined as brief unconsciousness or period of confusion or daze following a minor head injury with no more than a few moments of associated amnesia and no significant physical lesions. It may be followed by a constellation of symptoms including headaches, dizziness, irritability, anxiety, insomnia, hypersensitivity to noise, and hypochondriacal concerns, without specific cognitive deficits. Compensation neurosis plays a role in some such patients, but in a small percentage (13% in one report26) these psychoneurotic symptoms have no relation to financial or other gains, and often cannot readily be distinguished from psychoneuroses in other situations. Age here too makes a difference; the symptoms in persons beyond 50 years tend to exceed those in young adults, both in severity and in duration.
The careful and detailed studies of the past ten years have added greatly to our knowledge and to both diagnostic and therapeutic efficacy.26 Many more investigations need to be carried out, in a variety of ways and on more and larger groups of patients. The recent detailed monograph on reaction times by Van Zomeren27 exemplifies this approach. The monograph of Levin, Benton and Grossman12 suggests directions that might profitably be explored and types of approaches which have already shown their value. This monograph is recommended for individuals who wish to expand their knowledge of this subject.
1. The type and degree of behavioral changes following head injury generally correlates with the severity of the injury as measured by the durations of coma and of the associated periods of amnesia.
2. The Glasgow Coma Scale and other methods which have been devised to quantitate the behavioral effects of head injury have led to improved understanding of the processes involved and often enable the clinician to estimate prognosis.
3. Head injuries are four times more common in males than in females, and older individuals (over 50) commonly suffer more serious and longer lasting after-effects than young adults.
4. Clinical deficits following head injury reflect specific neural damage, as exemplified by deficits in memory, intellectual function, and perception. Whether post-traumatic psychoneurosis or psychosis may similarly be the result of focal damage is unclear.
5. The signs and symptoms of diffuse brain injury represent a complex of effects of multiple focal lesions.
1. Aird RB. Garouttc B: Injury and diseases of the nervous system, in Brahdy L (ed): Disease and Injury. Philadelphia, Lippincott, 1963.
2. Kalsbeek WD. McLaurin RL. Harris BSH III, et al: The national head and spinal cord injury survey: Major findings. J Neurosurg 1980; 53(suppl): 19-31.
3. Feild |H: Epidemiology of Head Injury in England and Wales: With Particular Application to Rehabilitation. Leicester, printed for HM Stationery Office by Wilsons, 1976.
4. Annegers |F, Kurland LT: The epidemiology of central nervous system trauma, in Odom GL ted): Central Nervous System Trauma Research Status Report, 1979. Washington. DC. NIH, Public Health Service, 1979.
5. Newcombe F: Missile Wounds of the Brain, a Study of Psychological Deficits. London, Oxford University Press, 1969.
6. Zimmerman RA. Bilaniuk LT. Genneralli T: Computed tomography of shearing injuries of the cerebral white matter. Radiology 1978; 127:393-396.
7. Teasdale G, iennett B: Assessment of coma and impaired consciousness: A practical scale. Lancet 1974; 2:81-84.
8. Levin HS, O'Donnell VM. Grossman RG: The Galveston orientation and amnesia test: A practical scale to assess cognition after head injury. J Nerve Ment Dis 1979; 167:675-684.
9. Yen JK, Bourke RS. Popp AJ, et al: Use of ethacrynic acid in the treatment of serious head injury, in Popp AI, Bourke RS, Nelson LR, et al (eds): Neural Trauma. New York. Raven Press. 1979.
10. Heiden JS, Small R, Caton W, et al: Severe head injury and outcome: A prospective study, in Popp AI, Bourke RS, Nelson LR, et al (eds): Neural Trauma. New York, Raven Press, 1979.
11. Russell WR: The Traumatic Amnesias. New York, Oxford University Press, 1971.
12. Levin HS, Benton AL, Grossman RG: Neurobehavioral Consequences of Closed Head Injury. New York, Oxford University Press, 1982.
13. Iennett B: Assessment of the severity of head injury. J Neurol Neurosurg Psychiatry 1976; 39:647-655.
14. Brooks DN: Long and short term memory in head injured patients. Cortex 1975; 1 1:329-340.
15. Buschke H, FuId PA: Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology 1974; 24:1019-1025.
16. Kimura D: Right temporal lobe damage. Arch Neurol 1963; 8:264-271.
17. Milner B: Clues to the cerebral organization of memory, in Buser PA. Rongeul-Buser(eds): Cerebral Correlates of Conscious Experience INSERM Symposium No. 6. New York. Elsevier North Holland Biomedical Press, 1978.
18. Brooks DN: Memory and head injury. J Nerv Ment Dis 1972; 155:350-355.
19. Najenson T, Sazbon L, Fiselzon J. et al: Recovery of communicative functions after prolonged traumatic coma. Scand J Rehabil Med 1978; 10: 15-21.
20. Sarno MT: The nature of verbal impairment after closed head injury. J Nerv Ment Dis 1980; 168:685-692.
21. Spreen O, Benton AL: Neurosensory Center Comprehensive Examination for Aphasia: Manual of Direction. Victoria, British Columbia, Neuropsychology Laboratory, University of Victoria, 1 966.
22. Zimmerman RA, Bilaniuk LT: Computed tomography in diffuse cerebral trauma, in Popp AJ, Bourke RS, Nelson LR, et al (eds): Neural Trauma. New York. Raven Press, 1979.
23. Levin HS, Grossman RG, Sarwar M, et al: Linguistic recovery after closed head injury. Brain and Language 1981; 12:360-374.
24. Hannay HJ, Levin HS, Kay M: Tachistoscopic visual perception after closed head injuries. J Clin Neuropsychol 1982;4:117-129.
25. Van Zomeren AH, Deelman BG: Long-term recovery of visual reaction time after closed head injury. J Neurol Neurosurg Psychiatry 1978; 41:452-457.
26. Odom GL (ed): Central Nervous System Trauma Research Status Report. Washington, DC. NINCDS, NIH. Public Health Service, 1979.
27. Van Zomeren AH: Reaction Time and Attention After Closed Head Injury. Toronto, Hogrefe International. 1981.
Figure 1. The Glasgow Coma Scale.