A l t e red St a t e s o f Consciousness in Small Animals Simon Platt,
BVM&S, MRCVS
KEYWORDS Consciousness Confusion Stupor Coma Intracranial pressure Small animals KEY POINTS Consciousness is best represented by both wakefulness and awareness. Abnormalities of consciousness indicate a brainstem and/or forebrain localization. Any disease that affects intracranial structures can cause abnormalities of consciousness. Severely impaired consciousness can represent a medical emergency. Immediate fluid therapy and oxygen therapy are the most successful supportive measures for acute impaired states of consciousness.
INTRODUCTION
The terms consciousness, confusion, stupor, unconsciousness, and coma have been endowed with so many different meanings that it is almost impossible to avoid ambiguity in their usage. The word consciousness is the most difficult of all to define. For practical and didactic purposes, consciousness is often described as having 2 main components: awareness and wakefulness. At present, there is no single marker of awareness, but its presence can be clinically deduced from behavioral signs, such as visual pursuit or responses to command. Wakefulness describes the state of arousal, often apparent by opened eyes. Abnormalities of consciousness usually indicate diseases or intoxications that result in dysfunction of the brainstem and/or the cerebrum. Clinical abnormalities may be acute or chronic in nature and may vary from subtle to profound dysfunction. Assessment of consciousness is based on an animal’s responses, either appropriate or inappropriate, to its environment, and stimuli, both normal and abnormal, within that environment. As such, familiarity with the range of normal responses of cats versus
Department of Small Animal Medicine & Surgery, College of Veterinary Medicine, University of Georgia, 501 DW Brooks Drive, Athens, GA 30602, USA E-mail address: [email protected] Vet Clin Small Anim 44 (2014) 1039–1058 http://dx.doi.org/10.1016/j.cvsm.2014.07.012 vetsmall.theclinics.com 0195-5616/14/$ – see front matter Ó 2014 Elsevier Inc. All rights reserved.
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dogs, young animals versus old animals, and highly active breeds, such as terriers, versus less-active giant breeds is important in the assessment of consciousness. STATES OF NORMAL AND IMPAIRED CONSCIOUSNESS
The following definitions aim to describe the states of consciousness in terms of awareness and wakefulness so that they can be practically identified and related to underlying disease of the nervous system (Table 1): A. Normal consciousness. This is the condition of the normal animal when awake. In this state, the animal is fully responsive. B. Confusion. The term confusion lacks precision but in general it denotes an inability to think with appropriate speed and clarity. This is obviously open to subjective interpretation in veterinary medicine, but it is proposed here as the term that describes an abnormal state of awareness because of its simplicity and its intuitive implication. Assessing an animal to be either normally aware versus confused relies on an interpretation of an animal’s behavior, which itself is defined as the observable response of an animal to environmental or specific stimuli (Fig. 1). Behavior suggestive of confusion includes getting trapped in corners or under furniture, unprovoked vocalization, staring at the floor or wall for protracted periods of time, and loss of house training. The words delirium and dementia have been inappropriately used in the veterinary literature to describe abnormal states of awareness. In human neurology, delirium describes a mental disturbance denoted by excitement, restlessness, and unprovoked vocalization often associated with hallucinations, whereas dementia is defined as impaired intellectual function involving memory and judgment, as well as changes in personality. Accurate assessment of these states in veterinary medicine is not obviously possible; additionally they Table 1 States of consciousness in animals State of Consciousness
Wakefulness
Awareness
Interpretation
Normal consciousness
Preserved
Preserved
No evidence of intracranial disease but it cannot be ruled out.
Drowsy
Reduced
Preserved
Possible primary brainstem or forebrain disease but systemic disease, intoxication, and even pain could be responsible. A drowsy and confused state would isolate the disease to the forebrain.
Confused
Preserved
Reduced
Isolates the disease to the forebrain. A drowsy and confused state also can be possible with this lesion localization.
Stupor
Absent
Absent
This indicates severe disease of the brainstem and/or bilateral cerebral hemispheres. The animal can be aroused with noxious stimulation.
Coma
Absent
Absent
As for stupor, this indicates severe disease of the brainstem and or bilateral cerebral hemispheres. The animal cannot be aroused with noxious stimulation but some cranial nerve reflexes may still be present if the brainstem is not involved.
Altered States of Consciousness in Small Animals
Fig. 1. (A) A 7-year-old boxer demonstrates abnormal consciousness. This could represent a drowsy state and/or a confused state. Without observing environmental interactions and responses, such an assessment could not be made. (B) A 3-year-old domestic short hair cat is “trapped” in a corner, which is one of several behavioral manifestations of a confused state.
do not determine a different or more specific lesion localization or a distinct set of differentials in comparison with the use of the more encompassing term confusion. C. Drowsiness. This term denotes a reduced ability to sustain a normally wakeful state without the application of external stimuli (see Fig. 1). Slow arousal is usually elicited by speaking to the animal or applying a tactile stimulus. A state of drowsiness does not necessarily imply primary dysfunction of the central nervous system (CNS), but disorders of the brainstem and occasionally bilateral cerebral hemisphere disease may be responsible. The terms lethargy, obtundation, and depression have synonymously and inappropriately been used in the veterinary literature to describe the state of drowsiness. Lethargy describes a lowered level of consciousness, with drowsiness, listlessness, and apathy; the latter obviously cannot be assessed in dogs and cats. Obtundation is defined as a state of mental blunting with mild to moderate reduction in alertness and a diminished sensation of pain, which cannot be accurately assessed in dogs and cats. Depression represents a mental state of altered mood characterized by feelings of sadness, despair, and discouragement, which obviously cannot be assessed in veterinary medicine. D. Stupor. This term describes an animal that is unconscious, essentially unresponsive to normal environmental stimuli, but is responsive to painful stimuli. Such cases either have a disease of or affecting (ie, toxicity) both cerebral hemispheres and more usually the brainstem. E. Coma. An animal in this state is unconscious and unresponsive to any stimulus, including noxious pain. As for stupor, diseases of or affecting bilateral hemispheres or the brainstem are suggested. NEURO-ANATOMICAL BASIS OF CONSCIOUSNESS
Clinicopathological correlation and neurophysiological experimentation have shown that coma is caused by diffuse bilateral cerebral hemisphere damage, failure of the ascending reticular activating system, or both.1,2 The reticular formation is composed of a network of both ascending and descending neuronal communications and forms an extensive component of the neuraxis in all mammals.2 The ascending component of the reticular system forms a diffuse midline system in the brainstem and spinal cord and receives input from all sensory modalities (except muscle and joint proprioception) and projects this information diffusely to the cerebral cortex via the thalamus. The ascending reticular formation arouses all areas of the cerebral cortex, resulting
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in a normal level of consciousness. Therefore, the ascending reticular formation is often referred to as the reticular activating system (RAS). Experimental work in animals suggests that the following structures play key roles in the maintenance and modulation of wakefulness: cholinergic nuclei in the upper brainstem and basal forebrain; noradrenergic nuclei, in particular the locus coeruleus; a histaminergic projection from the hypothalamus; and probably dopaminergic and serotonergic pathways arising from the brainstem.2 Additionally, hypocretins (orexins) are more recently described hypothalamic neuropeptides thought to have an important role in the regulation of sleep and arousal states.3 Much of the influence exerted by all of these pathways is mediated by the thalamus, which is regarded as the apex of the RAS, as well as a critical synaptic relay for most sensory pathways.2 The function of these activating structures is not confined to the maintenance of wakefulness: they are of profound importance to a wide range of interrelated functions, including motivation, attention, learning, and movement.4 Some specific contributions made by these and other structures to the regulation of conscious states have been defined. For example, the suprachiasmatic nucleus of the hypothalamus provides a timekeeper function.2 Additionally, transection experiments have established the key importance of cholinergic nuclei at the pontomesencephalic junction, the laterodorsal tegmental and pedunculopontine nuclei, in the reduction of consciousness during sleep.2 More caudally, the rostral pons and caudal midbrain make a critical contribution to the RAS and are important in mediating the effects of CNS depressants and stimulants. The true seat of consciousness is the cerebral cortex; however, the RAS is critical for adjusting the level of cerebral activity, and damage to either area or interruption of the communication between the RAS and the cerebrum will result in abnormal levels of wakefulness. Extensive bilateral dysfunction of cerebral hemisphere function is required to produce coma and therefore a unilateral hemisphere lesion will not result in coma unless there is secondary brainstem compression that compromises the ascending reticular activating system. Bilateral thalamic and hypothalamic lesions also cause coma by interrupting activation of the cortex.1 The speed of onset, site, and size of a brainstem lesion determine whether it results in coma, so brainstem infarction or hemorrhage often cause coma, whereas other brainstem conditions (eg, neoplasia) rarely do so. Drugs and metabolic disease produce coma by depression of both cortex and RAS function. In the assessment of the poorly responsive animal, it is important to analyze quality of the consciousness (normal vs confused) as well as the quantity. Normal behavior requires the complex interaction of numerous components of the thalamus and cerebral cortex. Of particular interest is the limbic system, which is associated with emotional and behavioral patterns in animals. It functions in the nonolfactory part of the rhinencephalon (the part of the brain once thought to be concerned entirely with olfactory functions). The name limbic (edge or border) is used because the nuclei that primarily comprise the nonolfactory rhinencephalon lie in 2 incomplete rings on the medial aspect of the telencephalon at its border with the diencephalon. The term now includes other anatomically distant nuclei, such as those in the brainstem. The major structures of the limbic system include the amygdaloid, hippocampus, and cingulate gyrus in the telencephalon, the thalamus and hypothalamus in the diencephalon, and the reticular formation of the mesencephalon. The function of the limbic system is to influence visceral motor activity, primarily through its influence on the hypothalamus. Neurons in this system receive projections from the olfactory, optic, auditory, exteroceptive, and interoceptive sensory systems. It is the portion of the brain in humans that is involved in basic drives, sexual activity, emotional experiences, memories, fears, and pleasures.
Altered States of Consciousness in Small Animals
NEUROLOGIC EVALUATION OF THE ANIMAL WITH IMPAIRED CONSCIOUSNESS
The clinician needs to determine what type of lesion is responsible for the impaired consciousness and its severity. The first component of a complete neurologic examination consists of general observations, including the level of consciousness. If possible, an animal should be allowed to move around freely so that its response to both the local environment and people can be assessed. This may be accomplished while the examiner is obtaining the pertinent history and presenting complaints from the owner. Using the Modified Glasgow Coma Scoring System
In humans, traumatic brain injury is graded as mild, moderate, or severe on the basis of the level of consciousness or the Glasgow Coma Scale.5–11 Mild traumatic brain injury in humans is usually the result of concussion, and full neurologic recovery routinely occurs. A patient with moderate traumatic brain injury is drowsy, and a patient with severe injury is stuporous or comatose. Patients with severe traumatic brain injury have a high risk of hypotension, hypoxemia, and brain swelling.6–11 If these sequelae are not prevented or managed properly, they can exacerbate the brain injury and increase the risk of death. The clinical point at which to initiate therapy for a veterinary patient with head trauma, the extent of appropriate therapy, and the length of time that such treatment is necessary are poorly documented. The effectiveness of specific treatment and the prognosis for any given animal will always be difficult to assess because of the multifactorial nature of the injury. A modification of the Glasgow Coma Scale used in humans has been proposed for use in veterinary medicine (Table 2).12 This scoring system enables grading of the initial neurologic status and serial monitoring of the patient with impaired consciousness. Although primarily investigated for its prognostic value in head trauma, this modified scale could be used to assess baseline function whatever the underlying cause of cerebral dysfunction, creating a baseline against which the patient can be monitored. Such a system can facilitate the assessment of prognosis, which is crucial information for both the veterinarian and owner. An almost linear correlation between this scoring system and short-term survival of dogs with head trauma has now been demonstrated.12 It should be noted that long-term survival and functional outcome have not been evaluated using these scales in dogs or cats. Each of the 3 categories of the examination (ie, level of consciousness, motor activity, brain stem reflexes) is assigned a score from 1 to 6. The level of consciousness provides information about the functional capabilities of the cerebral cortex and the reticular activating system in the brain stem.13 Levels of consciousness
The level of consciousness is the most reliable empiric measure of impaired cerebral function after head injury. Impairment of consciousness is stratified in terms of the responses to external stimuli, and serial records of these responses provide an important guide to treatment. Decreasing levels of consciousness indicate abnormal function of the cerebral cortex or interference with transmission of sensory stimuli by the reticular activating system. Human patients who arrive in a state of coma generally have bilateral or global cerebral abnormalities or severe brain stem injury and have a guarded prognosis.14 Limb movements, posture, and reflexes
Spontaneous and evoked limb movements are studied as part of the coma scale examination.12 It is important for the clinician to determine whether spinal cord injury or severe orthopedic abnormalities are present before extensive manipulation of the patient.
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Table 2 Small animal Modified Glasgow Coma Scale (MGCS) Assessment Parameter
Score
Motor activity Normal gait, normal spinal reflexes
6
Hemiparesis, tetraparesis, or decerebrate activity
5
Recumbent, intermittent extensor rigidity
4
Recumbent, constant extensor rigidity
3
Recumbent, constant extensor rigidity with opisthotonus
2
Recumbent, hypotonia of muscles, depressed or absent spinal reflexes
1
Brain stem reflexes Normal pupillary light reflexes and oculocephalic reflexes
6
Slow pupillary light reflexes and normal to reduced oculocephalic reflexes
5
Bilateral, unresponsive miosis with normal to reduced oculocephalic reflexes
4
Pinpoint pupils with reduced to absent oculocephalic reflexes
3
Unilateral, unresponsive mydriasis with reduced to absent oculocephalic reflexes
2
Bilateral, unresponsive mydriasis with reduced to absent oculocephalic reflexes
1
Level of consciousness Occasional periods of alertness and responsiveness to environment
6
Depression or delirium, capable of responding but response may be inappropriate
5
Semicomatose, responsive to visual stimuli
4
Semicomatose, responsive to auditory stimuli
3
Semicomatose, responsive only to repeated noxious stimuli
2
Comatose, unresponsive to repeated noxious stimuli
1
A score is given to each of 3 categories of the neurologic examination: motor activity, brain stem reflexes, and level of consciousness. Within each category, a score of 1 to 6 exists, representing the most severe to the mildest of clinical pictures. A total score can then be helpful (1) in estimating the severity of the initial condition, which determines the most appropriate level of therapy; (2) assessing the prognosis for survival within the first 72 hours; and (3) assessing the effect of therapy. From Platt SR, Radaelli ST, McDonnell JJ. The prognostic value of the modified Glasgow Coma Scale in head trauma in dogs. J Vet Intern Med 2001;15:581; with permission.
Motor activity may be affected by the animal’s level of consciousness; the best motor response detected is the most important. Animals that are not comatose, but have an altered state of consciousness, usually maintain some voluntary motor activity. Muscle tone is assessed by putting the limbs through a full range of passive movement, keeping in mind the possibility of a long-bone or joint fracture. The tendon reflexes are elicited; these reflexes have very little value in the diagnosis of acute cerebral injuries, but localized absence of tendon jerks may disclose a nerve injury. Exaggerated reflexes can be seen in all 4 limbs in patients with cerebral injury (or cervical spinal cord trauma), but severely affected comatose animals lose muscle tone and reflex activity. Opisthotonus with hyperextension of all 4 limbs is suggestive of decerebrate rigidity, which results from a midbrain lesion and is caused because the reticular formation in the brainstem facilitates gamma motor activity and the vestibulospinal system facilitates alpha motor neuron activity. Severe and acute injury rostral to these structures can result in their “release,” causing increased extensor tone of all limbs. This posture is occasionally seen in animals recumbent as a result of craniocerebral trauma, and can provide further information about the severity of the brain injury. Variable flexion and extension of the hind limbs is seen in rigidity with cerebellar injury accompanied by a normal level of consciousness; this is termed decerebellate rigidity (Fig. 2).14
Altered States of Consciousness in Small Animals
Fig. 2. A 9-year-old cat exhibits decrebellate rigidity. The thoracic limbs demonstrate increased extensor tone and the pelvic limbs demonstrate increased flexor tone, which is most classic for a severe and often acute lesion affecting the cerebellum. The animal’s consciousness may be unaffected if a pure cerebellar lesion is responsible.
Neuro-ophthalmologic examination Pupillary responses Proper assessment of the pupillary responses requires a bright
light in a dimmed room. The clinician should be aware that prior and ongoing ophthalmic disease of any nature, concomitant trauma to the eye, and the use of drugs, such as atropine, dopamine, and opioids, can all have effects on pupillary reactions that may be misleading. Pupil size, shape, and reactivity are recorded routinely during the initial examination and should be checked at frequent intervals thereafter (Table 3). Table 3 Anatomic interpretation of pupillary abnormalities Associated Findings
Injury
Ipsilateral Pupil
Oculomotor nerve
Dilated and fixed to direct light No consensual constriction from contralateral light but normal consensual constriction in contralateral pupil
Ptosis and ventrolateral strabismus
Optic nerve
Fixed to direct light Absent consensual constriction in contralateral pupil Normal consensual constriction from contralateral light
Spontaneous fluctuations in pupil size
Oculomotor and optic nerve
Dilated and fixed to direct light No consensual constriction from contralateral light and no consensual constriction in contralateral pupil
Ptosis and ventrolateral strabismus
Iris or ciliary body
Dilated and fixed to direct light No consensual constriction from contralateral light but normal consensual constriction in contralateral pupil
Often signs of orbital injury No strabismus
Cervical sympathetic pathway
Constricted and fixed or sluggish to direct light and contralateral light but normal consensual constriction in contralateral pupil
Ptosis
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The pupillary light reflex (PLR) is tested by shining a bright light into the pupil and assessing for pupillary constriction (direct reflex). The opposite pupil should constrict at the same time (consensual or indirect reflex). A slight dilation usually follows the initial pupillary constriction (pupillary escape) as a consequence of light adaptation of photoreceptors. The PLR involves an afferent arm and an efferent arm. The afferent arm of this reflex shares some common pathways (ipsilateral retina, optic nerve, optic chiasm, and contralateral optic tract) with part of the afferent arm of the menace response and visual placing (Fig. 3). These tests use different integration centers within the brain and different efferent pathways. The PLR does not test the animal’s vision and the cerebrum is not involved in the PLR pathway. The efferent arm of the PLR reflex is mediated by the parasympathetic portion of cranial nerve III (oculomotor nerve). Although axons involved in vision reach the conscious level after synapse with the lateral geniculate nucleus, the axons involved in the PLR synapse with a third neuron in the pretectal nucleus. Most of the axons arising from this nucleus decussate (cross over) again and synapse in the parasympathetic component of the oculomotor nucleus (ipsilateral to the stimulated eye) in the mesencephalon. There are also neurons that do not decussate and that project to the oculomotor nucleus on the contralateral side of the stimulated eye. The proportion of axons that decussate is higher than the ones that do not decussate, explaining why the direct response (constriction in the eye receiving the light stimulus) is greater than the consensual response (constriction in the eye not receiving the light stimulus). Combining the results of the menace response and PLR testing helps to localize the lesion as being within the common pathways or not. Pupillary abnormalities may be bilateral or unilateral. Mild size discrepancy between the 2 pupils (
BVM&S, MRCVS
KEYWORDS Consciousness Confusion Stupor Coma Intracranial pressure Small animals KEY POINTS Consciousness is best represented by both wakefulness and awareness. Abnormalities of consciousness indicate a brainstem and/or forebrain localization. Any disease that affects intracranial structures can cause abnormalities of consciousness. Severely impaired consciousness can represent a medical emergency. Immediate fluid therapy and oxygen therapy are the most successful supportive measures for acute impaired states of consciousness.
INTRODUCTION
The terms consciousness, confusion, stupor, unconsciousness, and coma have been endowed with so many different meanings that it is almost impossible to avoid ambiguity in their usage. The word consciousness is the most difficult of all to define. For practical and didactic purposes, consciousness is often described as having 2 main components: awareness and wakefulness. At present, there is no single marker of awareness, but its presence can be clinically deduced from behavioral signs, such as visual pursuit or responses to command. Wakefulness describes the state of arousal, often apparent by opened eyes. Abnormalities of consciousness usually indicate diseases or intoxications that result in dysfunction of the brainstem and/or the cerebrum. Clinical abnormalities may be acute or chronic in nature and may vary from subtle to profound dysfunction. Assessment of consciousness is based on an animal’s responses, either appropriate or inappropriate, to its environment, and stimuli, both normal and abnormal, within that environment. As such, familiarity with the range of normal responses of cats versus
Department of Small Animal Medicine & Surgery, College of Veterinary Medicine, University of Georgia, 501 DW Brooks Drive, Athens, GA 30602, USA E-mail address: [email protected] Vet Clin Small Anim 44 (2014) 1039–1058 http://dx.doi.org/10.1016/j.cvsm.2014.07.012 vetsmall.theclinics.com 0195-5616/14/$ – see front matter Ó 2014 Elsevier Inc. All rights reserved.
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dogs, young animals versus old animals, and highly active breeds, such as terriers, versus less-active giant breeds is important in the assessment of consciousness. STATES OF NORMAL AND IMPAIRED CONSCIOUSNESS
The following definitions aim to describe the states of consciousness in terms of awareness and wakefulness so that they can be practically identified and related to underlying disease of the nervous system (Table 1): A. Normal consciousness. This is the condition of the normal animal when awake. In this state, the animal is fully responsive. B. Confusion. The term confusion lacks precision but in general it denotes an inability to think with appropriate speed and clarity. This is obviously open to subjective interpretation in veterinary medicine, but it is proposed here as the term that describes an abnormal state of awareness because of its simplicity and its intuitive implication. Assessing an animal to be either normally aware versus confused relies on an interpretation of an animal’s behavior, which itself is defined as the observable response of an animal to environmental or specific stimuli (Fig. 1). Behavior suggestive of confusion includes getting trapped in corners or under furniture, unprovoked vocalization, staring at the floor or wall for protracted periods of time, and loss of house training. The words delirium and dementia have been inappropriately used in the veterinary literature to describe abnormal states of awareness. In human neurology, delirium describes a mental disturbance denoted by excitement, restlessness, and unprovoked vocalization often associated with hallucinations, whereas dementia is defined as impaired intellectual function involving memory and judgment, as well as changes in personality. Accurate assessment of these states in veterinary medicine is not obviously possible; additionally they Table 1 States of consciousness in animals State of Consciousness
Wakefulness
Awareness
Interpretation
Normal consciousness
Preserved
Preserved
No evidence of intracranial disease but it cannot be ruled out.
Drowsy
Reduced
Preserved
Possible primary brainstem or forebrain disease but systemic disease, intoxication, and even pain could be responsible. A drowsy and confused state would isolate the disease to the forebrain.
Confused
Preserved
Reduced
Isolates the disease to the forebrain. A drowsy and confused state also can be possible with this lesion localization.
Stupor
Absent
Absent
This indicates severe disease of the brainstem and/or bilateral cerebral hemispheres. The animal can be aroused with noxious stimulation.
Coma
Absent
Absent
As for stupor, this indicates severe disease of the brainstem and or bilateral cerebral hemispheres. The animal cannot be aroused with noxious stimulation but some cranial nerve reflexes may still be present if the brainstem is not involved.
Altered States of Consciousness in Small Animals
Fig. 1. (A) A 7-year-old boxer demonstrates abnormal consciousness. This could represent a drowsy state and/or a confused state. Without observing environmental interactions and responses, such an assessment could not be made. (B) A 3-year-old domestic short hair cat is “trapped” in a corner, which is one of several behavioral manifestations of a confused state.
do not determine a different or more specific lesion localization or a distinct set of differentials in comparison with the use of the more encompassing term confusion. C. Drowsiness. This term denotes a reduced ability to sustain a normally wakeful state without the application of external stimuli (see Fig. 1). Slow arousal is usually elicited by speaking to the animal or applying a tactile stimulus. A state of drowsiness does not necessarily imply primary dysfunction of the central nervous system (CNS), but disorders of the brainstem and occasionally bilateral cerebral hemisphere disease may be responsible. The terms lethargy, obtundation, and depression have synonymously and inappropriately been used in the veterinary literature to describe the state of drowsiness. Lethargy describes a lowered level of consciousness, with drowsiness, listlessness, and apathy; the latter obviously cannot be assessed in dogs and cats. Obtundation is defined as a state of mental blunting with mild to moderate reduction in alertness and a diminished sensation of pain, which cannot be accurately assessed in dogs and cats. Depression represents a mental state of altered mood characterized by feelings of sadness, despair, and discouragement, which obviously cannot be assessed in veterinary medicine. D. Stupor. This term describes an animal that is unconscious, essentially unresponsive to normal environmental stimuli, but is responsive to painful stimuli. Such cases either have a disease of or affecting (ie, toxicity) both cerebral hemispheres and more usually the brainstem. E. Coma. An animal in this state is unconscious and unresponsive to any stimulus, including noxious pain. As for stupor, diseases of or affecting bilateral hemispheres or the brainstem are suggested. NEURO-ANATOMICAL BASIS OF CONSCIOUSNESS
Clinicopathological correlation and neurophysiological experimentation have shown that coma is caused by diffuse bilateral cerebral hemisphere damage, failure of the ascending reticular activating system, or both.1,2 The reticular formation is composed of a network of both ascending and descending neuronal communications and forms an extensive component of the neuraxis in all mammals.2 The ascending component of the reticular system forms a diffuse midline system in the brainstem and spinal cord and receives input from all sensory modalities (except muscle and joint proprioception) and projects this information diffusely to the cerebral cortex via the thalamus. The ascending reticular formation arouses all areas of the cerebral cortex, resulting
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in a normal level of consciousness. Therefore, the ascending reticular formation is often referred to as the reticular activating system (RAS). Experimental work in animals suggests that the following structures play key roles in the maintenance and modulation of wakefulness: cholinergic nuclei in the upper brainstem and basal forebrain; noradrenergic nuclei, in particular the locus coeruleus; a histaminergic projection from the hypothalamus; and probably dopaminergic and serotonergic pathways arising from the brainstem.2 Additionally, hypocretins (orexins) are more recently described hypothalamic neuropeptides thought to have an important role in the regulation of sleep and arousal states.3 Much of the influence exerted by all of these pathways is mediated by the thalamus, which is regarded as the apex of the RAS, as well as a critical synaptic relay for most sensory pathways.2 The function of these activating structures is not confined to the maintenance of wakefulness: they are of profound importance to a wide range of interrelated functions, including motivation, attention, learning, and movement.4 Some specific contributions made by these and other structures to the regulation of conscious states have been defined. For example, the suprachiasmatic nucleus of the hypothalamus provides a timekeeper function.2 Additionally, transection experiments have established the key importance of cholinergic nuclei at the pontomesencephalic junction, the laterodorsal tegmental and pedunculopontine nuclei, in the reduction of consciousness during sleep.2 More caudally, the rostral pons and caudal midbrain make a critical contribution to the RAS and are important in mediating the effects of CNS depressants and stimulants. The true seat of consciousness is the cerebral cortex; however, the RAS is critical for adjusting the level of cerebral activity, and damage to either area or interruption of the communication between the RAS and the cerebrum will result in abnormal levels of wakefulness. Extensive bilateral dysfunction of cerebral hemisphere function is required to produce coma and therefore a unilateral hemisphere lesion will not result in coma unless there is secondary brainstem compression that compromises the ascending reticular activating system. Bilateral thalamic and hypothalamic lesions also cause coma by interrupting activation of the cortex.1 The speed of onset, site, and size of a brainstem lesion determine whether it results in coma, so brainstem infarction or hemorrhage often cause coma, whereas other brainstem conditions (eg, neoplasia) rarely do so. Drugs and metabolic disease produce coma by depression of both cortex and RAS function. In the assessment of the poorly responsive animal, it is important to analyze quality of the consciousness (normal vs confused) as well as the quantity. Normal behavior requires the complex interaction of numerous components of the thalamus and cerebral cortex. Of particular interest is the limbic system, which is associated with emotional and behavioral patterns in animals. It functions in the nonolfactory part of the rhinencephalon (the part of the brain once thought to be concerned entirely with olfactory functions). The name limbic (edge or border) is used because the nuclei that primarily comprise the nonolfactory rhinencephalon lie in 2 incomplete rings on the medial aspect of the telencephalon at its border with the diencephalon. The term now includes other anatomically distant nuclei, such as those in the brainstem. The major structures of the limbic system include the amygdaloid, hippocampus, and cingulate gyrus in the telencephalon, the thalamus and hypothalamus in the diencephalon, and the reticular formation of the mesencephalon. The function of the limbic system is to influence visceral motor activity, primarily through its influence on the hypothalamus. Neurons in this system receive projections from the olfactory, optic, auditory, exteroceptive, and interoceptive sensory systems. It is the portion of the brain in humans that is involved in basic drives, sexual activity, emotional experiences, memories, fears, and pleasures.
Altered States of Consciousness in Small Animals
NEUROLOGIC EVALUATION OF THE ANIMAL WITH IMPAIRED CONSCIOUSNESS
The clinician needs to determine what type of lesion is responsible for the impaired consciousness and its severity. The first component of a complete neurologic examination consists of general observations, including the level of consciousness. If possible, an animal should be allowed to move around freely so that its response to both the local environment and people can be assessed. This may be accomplished while the examiner is obtaining the pertinent history and presenting complaints from the owner. Using the Modified Glasgow Coma Scoring System
In humans, traumatic brain injury is graded as mild, moderate, or severe on the basis of the level of consciousness or the Glasgow Coma Scale.5–11 Mild traumatic brain injury in humans is usually the result of concussion, and full neurologic recovery routinely occurs. A patient with moderate traumatic brain injury is drowsy, and a patient with severe injury is stuporous or comatose. Patients with severe traumatic brain injury have a high risk of hypotension, hypoxemia, and brain swelling.6–11 If these sequelae are not prevented or managed properly, they can exacerbate the brain injury and increase the risk of death. The clinical point at which to initiate therapy for a veterinary patient with head trauma, the extent of appropriate therapy, and the length of time that such treatment is necessary are poorly documented. The effectiveness of specific treatment and the prognosis for any given animal will always be difficult to assess because of the multifactorial nature of the injury. A modification of the Glasgow Coma Scale used in humans has been proposed for use in veterinary medicine (Table 2).12 This scoring system enables grading of the initial neurologic status and serial monitoring of the patient with impaired consciousness. Although primarily investigated for its prognostic value in head trauma, this modified scale could be used to assess baseline function whatever the underlying cause of cerebral dysfunction, creating a baseline against which the patient can be monitored. Such a system can facilitate the assessment of prognosis, which is crucial information for both the veterinarian and owner. An almost linear correlation between this scoring system and short-term survival of dogs with head trauma has now been demonstrated.12 It should be noted that long-term survival and functional outcome have not been evaluated using these scales in dogs or cats. Each of the 3 categories of the examination (ie, level of consciousness, motor activity, brain stem reflexes) is assigned a score from 1 to 6. The level of consciousness provides information about the functional capabilities of the cerebral cortex and the reticular activating system in the brain stem.13 Levels of consciousness
The level of consciousness is the most reliable empiric measure of impaired cerebral function after head injury. Impairment of consciousness is stratified in terms of the responses to external stimuli, and serial records of these responses provide an important guide to treatment. Decreasing levels of consciousness indicate abnormal function of the cerebral cortex or interference with transmission of sensory stimuli by the reticular activating system. Human patients who arrive in a state of coma generally have bilateral or global cerebral abnormalities or severe brain stem injury and have a guarded prognosis.14 Limb movements, posture, and reflexes
Spontaneous and evoked limb movements are studied as part of the coma scale examination.12 It is important for the clinician to determine whether spinal cord injury or severe orthopedic abnormalities are present before extensive manipulation of the patient.
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Table 2 Small animal Modified Glasgow Coma Scale (MGCS) Assessment Parameter
Score
Motor activity Normal gait, normal spinal reflexes
6
Hemiparesis, tetraparesis, or decerebrate activity
5
Recumbent, intermittent extensor rigidity
4
Recumbent, constant extensor rigidity
3
Recumbent, constant extensor rigidity with opisthotonus
2
Recumbent, hypotonia of muscles, depressed or absent spinal reflexes
1
Brain stem reflexes Normal pupillary light reflexes and oculocephalic reflexes
6
Slow pupillary light reflexes and normal to reduced oculocephalic reflexes
5
Bilateral, unresponsive miosis with normal to reduced oculocephalic reflexes
4
Pinpoint pupils with reduced to absent oculocephalic reflexes
3
Unilateral, unresponsive mydriasis with reduced to absent oculocephalic reflexes
2
Bilateral, unresponsive mydriasis with reduced to absent oculocephalic reflexes
1
Level of consciousness Occasional periods of alertness and responsiveness to environment
6
Depression or delirium, capable of responding but response may be inappropriate
5
Semicomatose, responsive to visual stimuli
4
Semicomatose, responsive to auditory stimuli
3
Semicomatose, responsive only to repeated noxious stimuli
2
Comatose, unresponsive to repeated noxious stimuli
1
A score is given to each of 3 categories of the neurologic examination: motor activity, brain stem reflexes, and level of consciousness. Within each category, a score of 1 to 6 exists, representing the most severe to the mildest of clinical pictures. A total score can then be helpful (1) in estimating the severity of the initial condition, which determines the most appropriate level of therapy; (2) assessing the prognosis for survival within the first 72 hours; and (3) assessing the effect of therapy. From Platt SR, Radaelli ST, McDonnell JJ. The prognostic value of the modified Glasgow Coma Scale in head trauma in dogs. J Vet Intern Med 2001;15:581; with permission.
Motor activity may be affected by the animal’s level of consciousness; the best motor response detected is the most important. Animals that are not comatose, but have an altered state of consciousness, usually maintain some voluntary motor activity. Muscle tone is assessed by putting the limbs through a full range of passive movement, keeping in mind the possibility of a long-bone or joint fracture. The tendon reflexes are elicited; these reflexes have very little value in the diagnosis of acute cerebral injuries, but localized absence of tendon jerks may disclose a nerve injury. Exaggerated reflexes can be seen in all 4 limbs in patients with cerebral injury (or cervical spinal cord trauma), but severely affected comatose animals lose muscle tone and reflex activity. Opisthotonus with hyperextension of all 4 limbs is suggestive of decerebrate rigidity, which results from a midbrain lesion and is caused because the reticular formation in the brainstem facilitates gamma motor activity and the vestibulospinal system facilitates alpha motor neuron activity. Severe and acute injury rostral to these structures can result in their “release,” causing increased extensor tone of all limbs. This posture is occasionally seen in animals recumbent as a result of craniocerebral trauma, and can provide further information about the severity of the brain injury. Variable flexion and extension of the hind limbs is seen in rigidity with cerebellar injury accompanied by a normal level of consciousness; this is termed decerebellate rigidity (Fig. 2).14
Altered States of Consciousness in Small Animals
Fig. 2. A 9-year-old cat exhibits decrebellate rigidity. The thoracic limbs demonstrate increased extensor tone and the pelvic limbs demonstrate increased flexor tone, which is most classic for a severe and often acute lesion affecting the cerebellum. The animal’s consciousness may be unaffected if a pure cerebellar lesion is responsible.
Neuro-ophthalmologic examination Pupillary responses Proper assessment of the pupillary responses requires a bright
light in a dimmed room. The clinician should be aware that prior and ongoing ophthalmic disease of any nature, concomitant trauma to the eye, and the use of drugs, such as atropine, dopamine, and opioids, can all have effects on pupillary reactions that may be misleading. Pupil size, shape, and reactivity are recorded routinely during the initial examination and should be checked at frequent intervals thereafter (Table 3). Table 3 Anatomic interpretation of pupillary abnormalities Associated Findings
Injury
Ipsilateral Pupil
Oculomotor nerve
Dilated and fixed to direct light No consensual constriction from contralateral light but normal consensual constriction in contralateral pupil
Ptosis and ventrolateral strabismus
Optic nerve
Fixed to direct light Absent consensual constriction in contralateral pupil Normal consensual constriction from contralateral light
Spontaneous fluctuations in pupil size
Oculomotor and optic nerve
Dilated and fixed to direct light No consensual constriction from contralateral light and no consensual constriction in contralateral pupil
Ptosis and ventrolateral strabismus
Iris or ciliary body
Dilated and fixed to direct light No consensual constriction from contralateral light but normal consensual constriction in contralateral pupil
Often signs of orbital injury No strabismus
Cervical sympathetic pathway
Constricted and fixed or sluggish to direct light and contralateral light but normal consensual constriction in contralateral pupil
Ptosis
1045
1046
Platt
The pupillary light reflex (PLR) is tested by shining a bright light into the pupil and assessing for pupillary constriction (direct reflex). The opposite pupil should constrict at the same time (consensual or indirect reflex). A slight dilation usually follows the initial pupillary constriction (pupillary escape) as a consequence of light adaptation of photoreceptors. The PLR involves an afferent arm and an efferent arm. The afferent arm of this reflex shares some common pathways (ipsilateral retina, optic nerve, optic chiasm, and contralateral optic tract) with part of the afferent arm of the menace response and visual placing (Fig. 3). These tests use different integration centers within the brain and different efferent pathways. The PLR does not test the animal’s vision and the cerebrum is not involved in the PLR pathway. The efferent arm of the PLR reflex is mediated by the parasympathetic portion of cranial nerve III (oculomotor nerve). Although axons involved in vision reach the conscious level after synapse with the lateral geniculate nucleus, the axons involved in the PLR synapse with a third neuron in the pretectal nucleus. Most of the axons arising from this nucleus decussate (cross over) again and synapse in the parasympathetic component of the oculomotor nucleus (ipsilateral to the stimulated eye) in the mesencephalon. There are also neurons that do not decussate and that project to the oculomotor nucleus on the contralateral side of the stimulated eye. The proportion of axons that decussate is higher than the ones that do not decussate, explaining why the direct response (constriction in the eye receiving the light stimulus) is greater than the consensual response (constriction in the eye not receiving the light stimulus). Combining the results of the menace response and PLR testing helps to localize the lesion as being within the common pathways or not. Pupillary abnormalities may be bilateral or unilateral. Mild size discrepancy between the 2 pupils (
