The neurophysiology of concussion

Prog Neurobiol. 2002 Jul;67(4):281-344. doi: 10.1016/s0301-0082(02)00018-7.

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Animals
  • Brain Concussion* / etiology
  • Brain Concussion* / physiopathology
  • Electroencephalography
  • Evoked Potentials
  • Humans