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Decapitation in Rats: Latency to Unconsciousness and the ‘Wave of Death’

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The question whether decapitation is a humane method of euthanasia in awake animals is being debated. To gather arguments in this debate, obsolete rats were decapitated while recording the EEG, both of awake rats and of anesthetized rats. Following decapitation a fast and global loss of power of the EEG was observed; the power in the 13-100 Hz frequency band, expressing cognitive activity, decreased according to an exponential decay function to half the initial value within 4 seconds. Whereas the pre-decapitation EEG of the anesthetized animals showed a burst suppression pattern quite different from the awake animals, the power in the postdecapitation EEG did not differ between the two groups. This might indicate that either the power of the EEG does not correlate well with consciousness or that consciousness is briefly regained in the anesthetized group after decapitation. Remarkably, after 50 seconds (awake group) or 80 seconds (anesthetized group) following decapitation, a high amplitude slow wave was observed. The EEG before this wave had more power than the signal after the wave. This wave might be due to a simultaneous massive loss of membrane potentials of the neurons. Still functioning ion channels, which keep the membrane potential intact before the wave, might explain the observed power difference. Two conclusions were drawn from this experiment. It is likely that consciousness vanishes within seconds after decapitation, implying that decapitation is a quick and not an inhumane method of euthanasia. It seems that the massive wave which can be recorded approximately one minute after decapitation reflects the ultimate border between life and death. This observation might have implications in the discussions on the appropriate time for organ donation.
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... However, there remains very little scientific evidence showing that cervical dislocation produces a reliable and/or a humane death. 53 Assumptions that cervical dislocation offers a humane death arise from data extrapolated from the decapitation of rats, [54][55][56][57][58] and data surrounding the specific welfare impacts of cervical dislocation remain sparse in rodents. 53,59 This is particularly concerning given that cervical dislocation is very different from decapitation, with a different mode of action, and of course mice are not small rats. ...
... However, this claim remains highly controversial and unsubstantiated, and the assertion that such high frequency signals reflect pain and discomfort has been heavily criticised. 54,56,58 One strong counterargument comes from findings showing that high frequency EEG signals are also present whilst under general anaesthesia, 33,69,70 as well as during rapid eye movement (REM) sleep. 27 Moreover, it has also been argued that, following decapitation, rapid blood loss would result in hypoxia rendering the decapitated head unconscious in less than 2.7 s, 55 and that lack of blood supply would be unable to support ongoing brain activity. ...
... 27 Moreover, it has also been argued that, following decapitation, rapid blood loss would result in hypoxia rendering the decapitated head unconscious in less than 2.7 s, 55 and that lack of blood supply would be unable to support ongoing brain activity. 64 In subsequent EEG work, it took 17 s following decapitation for the EEG signal to become isoelectric, with the power of the frequency bands expressing cognitive activity (13-100 Hz) decreasing exponentially to less than 50% of baseline power, representative of an unconscious state, after 3.7 s. 58 This result was corroborated in 1992 by loss of consciousness reported in 3-6 s, 56 as well as disputed by a later study demonstrating that brain activity (EEG and VEP assessment) was sustained for relatively long periods following decapitation (15-20 s). 59 EEG and VEP assessment are useful indicators but have limitations to their use. ...
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Rodents are the most widely used species for scientific purposes. A critical pre-requisite of their use, based on utilitarian ethical reasoning, is the provision of a humane death when necessary for scientific or welfare grounds. Focussing on the welfare challenges presented by current methods, we critically evaluate the literature, consider emerging methodologies that may have potential for refinement and highlight knowledge gaps for future research. The evidence supports the conclusion that scientists and laboratory personnel should seek to avoid killing laboratory rodents by exposing them to carbon dioxide (CO 2 ), unless exploiting its high-throughput advantage. We suggest that stakeholders and policymakers should advocate for the removal of CO 2 from existing guidelines, instead making its use conditionally acceptable with justification for additional rationale for its application. With regards to physical methods such as cervical dislocation, decapitation and concussion, major welfare concerns are based on potential inaccuracy in application and their susceptibility to high failure rates. There is a need for independent quality-controlled training programmes to facilitate optimal success rates and the development of specialist tools to improve outcomes and reliability. Furthermore, we highlight questions surrounding the inconsistent inclusion criteria and acceptability of physical methods in international regulation and/or guidance, demonstrating a lack of cohesion across countries and lack of a comprehensive ‘gold standard’ methodology. We encourage better review of new data and championing of open access scientific resources to advocate for best practice and enable significant changes to policy and legislation to improve the welfare of laboratory rodents at killing.
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Since the development of the infamous guillotine in the French Revolution, physicians have debated how long consciousness persists in decapitated heads. Fueled by anecdotes of severed heads that blink, blush, and appear to retain intelligence, numerous experiments have investigated this macabre subject for nearly 250 years. In this paper, we examine the evidence, both historical and modern, and ultimately conclude that, while the truth may never be fully known, all evidence appears to indicate that loss of consciousness appears to occur within seconds of decapitation. The rumors that circulated through the European consciousness during the Terror of the French Revolution appear to be just that - curious urban legends from an awed and terrified public.
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The question of humaneness of decapitation per se has been considered. The time required for the oxygen tension in decapitated rat brain to decline to a level at which the brain becomes unconscious was estimated to be 2.7 sec. Assuming that decapitation is a powerful arousal stimulus and that the resulting EEG activation (low voltage, fast activity) indicates a conscious awareness of pain and distress the maximum time the pain and distress could be perceived would be 2.7 sec. Hence, decapitation of rats per se may be considered humane.
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It has been debated whether or not decapitation of conscious animals is a humane procedure. This problem may be clarified on the basis of recent research that has indicated that neocortical low voltage fast activity (LVFA) and hippocampal rhythmical slow activity (RSA) can result from activity in either the cholinergic corticipetal projections from the basal forebrain or the serotonergic corticipetal projections from the brainstem. These inputs appear to produce, respectively, atropine-sensitive LVFA and RSA and atropine-resistant LVFA and RSA. In waking animals, atropine-resistant LVFA and RSA occur only in close correlation with motor activities such as spontaneous changes in posture, walking or struggling (Type 1 behavior). Painful stimuli readily elicit both Type 1 behavior and LVFA and RSA in atropine-treated rats. Atropine-sensitive LVFA and RSA may occur in anesthetized as well as in conscious animals, but atropine-resistant LVFA and RSA are generally absent during anesthesia. In the experiments reported here, rats were decapitated: (1) in the normal waking state; (2) after pretreatment with atropine or scopolamine; or (3) following induction of anesthesia with ethyl ether. Clear hippocampal RSA and neocortical LVFA were observed in conditions 1 and 3 but not in condition 2. It is concluded: (A) that atropine-sensitive LVFA and RSA are not good indices of conscious perception of pain since these waveforms occur during anesthesia as well as in the waking state; and (B) that the cerebral reaction to decapitation does not resemble the usual cerebral reaction to painful stimuli. This is consistent with the view that decapitation is not inhumane.