Review
The neurophysiology of concussion

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Abstract

Cerebral concussion is both the most common and most puzzling type of traumatic brain injury (TBI). It is normally produced by acceleration (or deceleration) of the head and is characterized by a sudden brief impairment of consciousness, paralysis of reflex activity and loss of memory. It has long been acknowledged that one of the most worthwhile techniques for studying the acute pathophysiology of concussion is by the recording of neurophysiological activity such as the electroencephalogram (EEG) and sensory evoked potentials (EPs) from experimental animals. In the first parts of this review, the majority of such studies conducted during the past half century are critically reviewed. When potential methodological flaws and limitations such as anesthetic protocols, infliction of multiple blows and delay in onset of recordings were taken into account, two general principles could be adduced. First, the immediate post-concussive EEG was excitatory or epileptiform in nature. Second, the cortical EP waveform was totally lost during this period. In the second parts of this review, five theories of concussion which have been prominent during the past century are summarized and supportive evidence assessed. These are the vascular, reticular, centripetal, pontine cholinergic and convulsive hypotheses. It is concluded that only the convulsive theory is readily compatible with the neurophysiological data and can provide a totally viable explanation for concussion. The chief tenet of the convulsive theory is that since the symptoms of concussion bear a strong resemblance to those of a generalized epileptic seizure, then it is a reasonable assumption that similar pathobiological processes underlie them both. Further, it is demonstrated that EPs and EEGs recorded acutely following concussive trauma are indeed the same or similar to those obtained following the induction of a state of generalized seizure activity (GSA). According to the present incarnation of the convulsive theory, the energy imparted to the brain by the sudden mechanical loading of the head may generate turbulent rotatory and other movements of the cerebral hemispheres and so increase the chances of a tissue-deforming collision or impact between the cortex and the boney walls of the skull. In this conception, loss of consciousness is not orchestrated by disruption or interference with the function of the brainstem reticular activating system. Rather, it is due to functional deafferentation of the cortex as a consequence of diffuse mechanically-induced depolarization and synchronized discharge of cortical neurons. A convulsive theory can also explain traumatic amnesia, autonomic disturbances and the miscellaneous collection of symptoms of the post-concussion syndrome more adequately than any of its rivals. In addition, the symptoms of minor concussion (a.k.a. being stunned, dinged, or dazed) are often strikingly similar to minor epilepsy such as petit mal. The relevance of the convulsive theory to a number of associated problems is also discussed. These include the relationship between concussion and more serious types of closed head injury, the utility of animal models of severe brain trauma, the etiology of the cognitive deficits which may linger long after a concussive injury, the use of concussive (captive bolt) techniques to stun farm animals prior to slaughter and the question of why some animals (such as the woodpecker) can tolerate massive accelerative forces without being knocked out.

Introduction

Cerebral concussion is a short-lasting disturbance of neural function typically induced by a sudden acceleration or deceleration of the head usually without skull fracture (Trotter, 1924, Denny-Brown and Russell, 1941, Symonds, 1962, Ward, 1966, Walton, 1977, Shetter and Demakas, 1979, Plum and Posner, 1980, Bannister, 1992, Rosenthal, 1993, Label, 1997). Falls, collisions, physical assaults, road traffic accidents, contact sports such as hockey, football and boxing as well as skiing, horseback riding and bicycle accidents are among the chief causes of concussion (Kraus and Nourjah, 1988). Concussion is not only the most common and familiar type of traumatic brain injury (TBI), but also one of the most puzzling of neurological disorders. The mystery lies not in the diagnosis of the condition, about which there is little dispute, but rather in the nature of its pathophysiology. The most dramatic aspect of concussion is an abrupt loss of consciousness with the patient dropping motionless to the ground and possibly appearing to be dead. This is usually quite brief, typically lasting just 1–3 min, and is followed by a spontaneous recovery of awareness. Definitions of concussion are almost always qualified by the statement that the loss of consciousness can occur in the absence of any gross damage or injury visible by light microscopy to the brain (Trotter, 1924, Denny-Brown and Russell, 1941, Friede, 1961, Ward, 1966, Nilsson et al., 1977, Shetter and Demakas, 1979, Plum and Posner, 1980, Ropper, 1994). While neuropathological changes may frequently occur, they are neither consistently present nor necessarily associated with the induction of concussion. This implies that concussion is a disorder of function rather than structure (Verjaal and Van ’T Hooft, 1975). This transient comatose state is also associated with a variety of more specific but less prominent signs and symptoms, not all of which may be invariably present. Judging by clinical observations as well as experimental animal studies, these include respiratory arrest or apnea, abolition of various reflex functions including corneal, pupillary and withdrawal responses, relatively prompt flaccidity of the musculature with the patient collapsing into a heap, ephemeral convulsive spasms, irregularities of heart rate including both bradycardia and tachycardia, alterations in cerebral blood flow (CBF) and fluctuations in blood pressure. Upon regaining consciousness, headache, nausea, dizziness, vomiting, malaise, restlessness, irritability and confusion may all be commonly experienced.

Notwithstanding the symptoms outlined above, the most significant effect of concussion besides loss of awareness is traumatic amnesia (Russell and Nathan, 1946, Symonds, 1962, Fisher, 1966, Benson and Geschwind, 1967, Yarnell and Lynch, 1970, Russell, 1971). There appears to be an intimate link between amnesia and concussion so much so that if a patient claims no memory loss, it is unlikely that concussion has occurred (Denny-Brown and Russell, 1941, Verjaal and Van ’T Hooft, 1975). Traumatic amnesia can be split into two components. Pre-traumatic or retrograde amnesia refers to loss of memory for events which transpired just prior to the concussion. Post-traumatic or anterograde amnesia applies to loss of memory for events after consciousness has been regained. It is often assumed that the severity of a concussive blow can be measured by the duration of post-traumatic amnesia (Russell, 1971). It has frequently been pointed out that any adequate theory of the pathobiology of concussion must be able to account for not only loss of consciousness but also for its other multifarious symptoms, especially the loss of memory (Ommaya and Gennarelli, 1974, Verjaal and Van ’T Hooft, 1975). The failure to cope with traumatic amnesia is one of the rocks on which many theories of concussion seem to founder.

One conspicuous feature of concussion is the number of symptoms which may linger long after the head injury has occurred and its acute effects resolved. This potpourri of residual symptoms has been exhaustively catalogued and investigated and is usually described as the post-concussion or post-traumatic syndrome (Strauss and Savitsky, 1934, Taylor, 1967, Kay et al., 1971, Merskey and Woodforde, 1972, Merritt, 1973, Martin, 1974, Symonds, 1974, Rutherford et al., 1977, Walton, 1977, Plum and Posner, 1980, Wrightson and Gronwall, 1981, McMillan and Glucksman, 1987, Hugenholtz et al., 1988, Lishman, 1988, Lowdon et al., 1989, Leininger et al., 1990, Montgomery et al., 1991, Barth et al., 1996, Rizzo and Tranel, 1996). Among the most common features of the post-concussion syndrome are headache, giddiness or vertigo, a tendency to fatigue, irritability, anxiety, aggression, insomnia and depression. These may be associated with a deterioration in work performance and a loss of social skills. In addition, there is a general cognitive impairment involving difficulties in recalling material, problems with concentration, inability to sustain effort and lack of judgment.

Although ostensibly a simple straightforward form of head injury, the study of concussion is distinguished by many unresolved issues. Some of these are summarized further. The sudden mechanical loading of the head associated with the concussive impact may cause temporary depression of the skull, movement of the head about the axis of the neck, abrupt displacement and rotational movements of the brain within the skull and generation of intracranial pressure (ICP) gradients. Such biomechanical events set up by the concussive blow may ultimately result in stretching, tearing, compression, or deformation injuries to the neural tissue. Disentangling which one, or combination of these factors is ultimately responsible for initiating a state of concussion has proven an arduous task.

A second problem concerns the relationship between transient concussion and more severe kinds of closed head injury in which the period of coma is prolonged. In other words, does concussion have a relatively unique pathogenesis or does it just differ quantitatively from more severe types of head trauma? (Plum and Posner, 1980). If it is the latter, this would suggest that concussion shares the same basic structural or functional injury as more severe brain injury but differs with respect to the degree of damage and potential for recovery. The quantitative viewpoint was strongly advocated in a famous paper by Sir Charles Symonds published 40 years ago (Symonds, 1962). In this, Symonds argued that “concussion should not be confined to cases in which there is immediate loss of consciousness with rapid and complete recovery but should include the many cases in which the initial symptoms are the same but with subsequent long-continued disturbance of consciousness, often followed by residual symptoms … Concussion in the above sense depends upon diffuse injury to nerve cells and fibres sustained at the moment of the accident. The effects of this injury may or may not be reversible.” Although this viewpoint has been very influential (e.g. Ommaya and Gennarelli, 1974), there is still no consensus on the quantitative versus qualitative dispute (Plum and Posner, 1980, McIntosh et al., 1996).

As described above, concussion is classically defined as occurring without overt morphological damage. Be that as it may, numerous experimental animal studies (and even some clinical data) have documented how histopathological changes in the brain of varying severity and permanence may often accompany concussion. Many of these have been summarized by Nilsson et al. (1977) and Shetter and Demakas (1979) and more recently by Dixon and Hayes (1995) and Povlishock (1995). They quote a multitude of examples where post-concussive examination of the brain has revealed evidence of microscopic and hemorrhagic lesions, neuronal loss and chromatolysis, as well as axonal damage. It is still unclear what, if any, role such organic injury plays in the pathogenesis of concussion. Some have been thought to represent the actual substrate of concussion. Alternately, they may be just a form of neuropathological epiphenomena. At most, these may provide an insight into its site of action. At least, they may be merely an artifact of the particular type of head injury device used (Shetter and Demakas, 1979).

Another enduring controversy concerns the status of the post-concussion syndrome. The persistence of those symptoms after even a mild head injury has led to the suspicion that their origin may be psychogenic rather than organic. Further, such a cluster of symptoms could be exacerbated by the possibility of malingering, neurosis or compensation claims. Nevertheless, careful neuropsychological testing has added weight to the belief that the post-concussion syndrome largely does reflect some kind of residual organic damage. Among the innovative research in this area was that of Gronwall and Wrightson, 1974, Gronwall and Wrightson, 1975. They used the paced auditory serial addition task (PASAT) to demonstrate that rate of information processing was slowed in patients who had sustained a concussion. Subsequent recovery in performance tended to correlate with the resolution of post-traumatic symptoms. Unfortunately, the neurogenesis of this sort of deficit in cognitive function and its related psychosocial symptoms still remains to be elucidated (Label, 1997).

The essential mystery of concussion does not pertain to an understanding of its biomechanics, nor to why it possesses amnesic properties, nor to the etiology of the post-traumatic syndrome, nor to its relationship to other forms of closed head injury, nor to the significance of any neuropathological changes which may accompany it. Rather, it is the paradox of how such a seemingly profound paralysis of neuronal function can occur so suddenly, last so transiently, and recover so spontaneously. As Symonds (1974) has again pointed out, no demonstrable lesion such as “laceration, edema, hemorrhage, or direct injury to the neurons” could account for such a pattern of loss and recovery of consciousness and cerebral function. The almost instantaneous onset of a concussive state following the blow, its striking reversibility, the seeming absence of any necessary structural change in brain substance plus the inconsistency of any neuropathology which may occur are all compatible with the conception of concussion as fundamentally a physiological disturbance. If this is so, then one of the most appropriate means to gain access to the acute pathophysiological processes would be by the recording of neurophysiological activity such as the electroencephalogram (EEG) and sensory evoked potentials (EPs) following concussion in experimental animals. Both of these are non-invasive measures of cerebral activity and so should be quite readily obtained during a concussive episode. It is a principal purpose of the present article to review the many studies which have attempted to measure the effects of experimental concussion on both the EEG and sensory EPs.

Section snippets

Historical background

The origin of the concept of cerebral concussion is shrouded in confusion. The term itself is comparatively modern, having been coined in the 16th century. According to the Oxford English Dictionary, the word concussion is derived from the Latin concutere. It refers to a clashing together, an agitation, disturbance or shock of impact. The term concussion therefore conveys the idea that a violent physical shaking of the brain is responsible for the sudden temporary loss of consciousness. It is,

The biomechanics of concussion

Any attempt to quantify the biomechanics of even a comparatively simple accelerative-type of head injury is still a formidably difficult task. Numerous factors or considerations need to be taken into account whether dealing with clinical concussion or experimental animal models. These could include: (1) skull shape, size and geometry; (2) density and mass of neural tissue; (3) thickness of scalp and skull; (4) extent, nature and direction of the concussive blow; (5) head–body relationships; and

Background

The EEG embodies the spontaneous rhythmic bioelectrical potentials which arise from the cortex. The exact electrogenesis of the EEG still remains uncertain (Lopes da Silva, 1991). Nevertheless, a common understanding is that it reflects the temporal and spatial summation of slow post-synaptic dendritic potentials especially those associated with pyramidal neurons (Schaul, 1998). The EEG may be synchronized or desynchronized depending upon the operation of subcortical pacemakers or by intrinsic

The vascular hypothesis

The vascular hypothesis is the oldest of the formal attempts to explain the nature of concussion but little attention is now paid to it. The theory held sway for the best part of a century (Symonds, 1962) and Denny-Brown and Russell (1941) have traced its antecedents in the latter part of the 19th century. Probably its last major proponent was Scott (1940) whose studies of head trauma in the dog were summarized earlier (Section 2). The vascular theory endured for a lengthy period despite early

Why doesn’t the woodpecker knock itself out?

While a wide variety of vertebrates seem to be susceptible to a concussive blow, a diverse minority are reputed to be virtually immune. These range from birds such as the nuthatch and woodpecker to mammals such as the billygoat and ram. These animals are believed to be able to routinely withstand accelerative or decelerative forces one hundred times greater than can be tolerated by humans (Ropper, 1994). The question of why some animals are invulnerable to concussive trauma is not merely of

Conclusions

All the five theories of concussion discussed in the present review have been current at times during the past century. They by no means represent an exhaustive list nor should they be considered mutually exclusive. As outlined, the various explanations often overlap one another to a greater or lesser extent. All five offer potentially valuable insights into the pathogenesis of concussion. All or most can supply a reasonable explanation for at least some of the elements of concussion.

Acknowledgements

Preparation of this review was funded by a grant from the Julius Brendel Trust. The author thanks: Dr. Richard Frith, Chairman of the Julius Brendel Trust, Professor Mark Cannell for the opportunity to write this review, Mrs. Jane Utting and Mrs. Rachel McAleer for help in preparation of the manuscript.

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