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Superior paraolivary nucleus in the pigmented guinea pig: separate classes of neurons project to the inferior colliculus and the cochlear nucleus.

The superior paraolivary nucleus is a large component of the superior olivary complex in rodents and a major source of input to the inferior colliculi and the cochlear nuclei. In the present study, retrograde transport of the fluorescent tracers Fluoro-Gold, Fluoro-Ruby (tetramethyl rhodamine conjugated to dextran), fluorescein-coated microspheres, and Fast Blue were used to reveal the morphology and collateral projection patterns of cells in the superior paraolivary nucleus. The ascending projections to the inferior colliculus from the superior paraolivary nucleus arise mainly from round, multipolar cells, including large cells that project exclusively to the inferior colliculi and not to the cochlear nuclei. Projections to the ipsilateral and contralateral inferior colliculi arise from cells with similar morphology and, in fact, many of the cells that project contralaterally project ipsilaterally as well. Projections to the ipsilateral and contralateral cochlear nuclei arise primarily from cells that do not have collicular projections. On average, the somas of these cells are significantly smaller and more elongated than those that project to the inferior colliculi. Overlap between these ascending and descending systems is restricted to a small percentage of cells that send collateral projections to both the ipsilateral cochlear nucleus and the ipsilateral inferior colliculus. These cells are small and moderately elongated. Thus the ascending and descending projections examined here arise largely from different cells that belong to different morphological classes.

Animals↗

Short-latency auditory evoked potentials in the monkey. II. Intracranial generators.

The generators of the short-latency auditory evoked potentials (SLAEPs) in the monkey have been defined by intracranial mapping from cochlea to auditory cortex. SLAEP components other than 1a and the slow negativity (SN) following wave 7 derive from compound action potentials propagated in subcortical auditory pathways. The component generators are complex due to the presence of two bursts of activity in the eighth nerve, to the fact that the ascending auditory fibers both synapse on and bypass specific relay nuclei, and to the differences in orientation of segments of the auditory pathways. Most SLAEP components recorded at the surface reflect the summation of activity from multiple generators. However, much of the activity seen within subcortical structures cannot be traced to the surface of the brain. Component 1a is identified with the cochlear summating potential, while 1b reflects the initial afferent volley in the distal portion of the eighth nerve. Component 2 represents the initial depolarization of the eighth nerve terminals within the ipsilateral cochlear nucleus. Component 3h reflects the second volley of activity in the distal portion of the eighth nerve and the outflow of the cochlear nucleus which decussates in the trapezoid body. Component 3v represents the initial cochlear nucleus outflow volley ascending the lateral lemniscus. Component 4 principally reflects the second volley of activity within the eighth nerve terminals, and outflow from the ipsilateral superior olivary complex ascending in that lateral lemniscus, with a possible contribution from activity in the contralateral CNC. Component 5 represents the outflow of the contralateral superior olivary complex ascending in that lateral lemniscus. Component 6 reflects another volley from the ipsilateral superior olivary complex ascending in that lateral lemniscus, as well as outflow from both inferior colliculi propagating in their brachii. The generators of component 7 are the most complex encountered, representing volleys in both lateral lemnisci, activity of the contralateral inferior colliculus, and activity in both auditory radiations. A component that follows wave 7, seen best in mastoid-to-mastoid recording linkage, represents outflow from both inferior colliculi propagating in their brachia. Components 8 and 9 principally reflect propagated action potentials in the auditory radiations bilaterally, with an additional contribution from activity of both inferior colliculi. The SN mainly represents volume-conducted postsynaptic potentials from both inferior colliculi and cochlear nuclei.

Animals↗

[Participation of the auditory centers of Rhinolophus ferrum-equinum in echolocational tracking of a moving target].

Behavioral and bioacoustic techniques were used to investigate the role of the auditory cortex and inferior colliculi in echolocative detection and tracking of moving targets by the greater horseshoe bat as well as their role in the regulation of vocal apparatus. It is demonstrated that complete bilateral auditory cortex destruction leads to considerable and irreversible changes in the process of tracking of moving targets but produce no detectable effect on the functioning of the vocal apparatus. Complete bilateral destruction of the inferior colliculi causes a loss of responses to moving targets (an artificial target or an insect). Animals with bilaterally destructed inferior colliculi show drastic changes in spectra of their echolocation calls manifested as occurence of multiple high- and low-frequency spectral components. The data suggest that the inferior colliculi of the midbrain are directly involved in echolocative tracking of moving targets and in matching of reception-emitting system of the bat. Participation of the auditory cortex in the process of echolocative detection of moving targets involves optimization of the echolocation system performance.

Animals↗

Projections from the ventral cochlear nucleus to the inferior colliculus and the contralateral cochlear nucleus in guinea pigs.

Multipolar cells in the ventral cochlear nucleus are the source of projections to numerous brainstem auditory nuclei, including the contralateral and ipsilateral inferior colliculi and the contralateral cochlear nucleus. Multiple fluorescent tracers were used to label the multipolar cells that project to each of these targets. Following injections of different tracers into each target, the ventral cochlear nucleus was examined for the presence of cells that contained more than one tracer. Such cells were never observed. In contrast, double-labeled cells were common in the dorsal cochlear nucleus, where cells frequently contained the two tracers that were injected into the ipsilateral and contralateral inferior colliculi. The distribution and somatic morphology of cells in the ventral cochlear nucleus that project to each of the three targets were examined. Each population contained cells with somas that ranged in shape from elongated to rounded, but there were differences in soma size. Projections to the ipsilateral and contralateral inferior colliculi arise predominantly from small to medium-sized cells, the average size being slightly less for cells with projections to the ipsilateral colliculus. Projections to the contralateral cochlear nucleus arise from cells with somas that range in size from small to large, including cells much larger than those that projected to either inferior colliculus. On the basis of these results, we conclude that projections from the ventral cochlear nucleus to the ipsilateral and contralateral inferior colliculi and to the contralateral cochlear nucleus arise in three different populations of multipolar cells.

Analysis of Variance↗

Ascending projections to the inferior colliculus following unilateral cochlear ablation in the neonatal gerbil, Meriones unguiculatus.

We evaluated the consequences of neonatal cochlear destruction upon ascending projections to the inferior colliculi. Unilateral cochlear ablations were performed in both neonatal and adult gerbils. Four to 12 months later, the inferior colliculus (IC) was examined physiologically and injected unilaterally with horseradish peroxidase (HRP). The number of labeled cells was determined bilaterally in all three divisions of cochlear nucleus (CN) and in the medial superior olive (MSO). In both experimental groups, transneuronal changes within the deafferented CN were greater in the ventral divisions than in the dorsal division. On the unoperated side the magnitude of projections from CN to the inferior colliculi was altered in animals lesioned as neonates. Following HRP injections into the IC on the unoperated side, the number of ipsilaterally labeled cells in CN (unoperated side) was significantly greater in the neonatal experimental group than in adult experimental and control animals. These anatomical changes were accompanied by increased ipsilaterally evoked excitatory activity recorded in the IC on the unoperated side. Following HRP injections into the IC on the ablated side, the number of contralaterally labeled cells in CN (unoperated side) was significantly reduced in animals lesioned as neonates as compared with control animals. The number of labeled cells in ipsilateral MSO was not significantly different across groups. Our interpretation is that unilateral cochlear ablation in neonatal gerbils results in an increase in the magnitude of ipsilateral projections and a decrease in the magnitude of contralateral projections from CN on the unoperated side to the inferior colliculi. These data suggest that the normal pattern of innervation of the IC results, in part, from interactions among afferent projections.

Animals↗

Effects of recurrent hypoglycemia on brainstem function in diabetic BB rats: protective adaptation during acute hypoglycemia.

To determine whether antecedent recurrent hypoglycemia protects the brain from the adverse effects of a standardized hypoglycemic stimulus, we implanted electrodes in the inferior colliculi of diabetic rats to directly record inferior colliculi auditory-evoked potentials (ICEPs). Awake, chronically catheterized BB rats were studied after 2 weeks of insulin therapy designed to produce either chronic hyperglycemia (hyper-DM, glycated hemoglobin 7.6 +/- 0.4%) or recurrent hypoglycemia (hypo-DM, glycated hemoglobin 6.2 +/- 0.7%), and the results were compared with those observed in nondiabetic rats. When plasma glucose was lowered to and clamped at 2.8 mmol/l, the release of catecholamines was suppressed in the hypo-DM rats (epinephrine: 2.5 +/- 0.4 nmol/l) as compared with hyper-DM and the nondiabetic rats (9.3 +/- 2.3 and 32.7 +/- 6.1 nmol/l, respectively). ICEP latency was significantly delayed in hyper-DM and nondiabetic rats (P < 0.001), but it was unchanged in hypo-DM rats. A more pronounced reduction in plasma glucose (2.0 mmol/l), however, provoked a greater adrenergic response than that seen at 2.8 mmol/l and delayed ICEP latency by 23% in a separate group of hypo-DM animals. These data demonstrate that antecedent recurrent hypoglycemia attenuates the brainstem dysfunction associated with mild to moderate, but not severe, hypoglycemia in diabetic rats. This phenomenon may contribute to the alterations in hypoglycemia counterregulation seen in diabetic patients during intensive insulin therapy.

Acute Disease↗

Collateral innervation of the inferior colliculus in the North American opossum: a study using fluorescent markers in a double-labeling paradigm.

The innervation of the opossum inferior colliculus was investigated using the retrograde transport of fluorescent markers in a double-labeling paradigm. True Blue was injected into one inferior colliculus while Nuclear Yellow was placed into the other. Many single-labeled neurons were found in all of the brainstem and cortical areas previously labeled by comparable injections of HRP. When the two injections of fluorescent markers were bilaterally symmetrical within the inferior colliculi, double-labeled neurons were numerous in the medial and lateral superior olivary nuclei. Only a few double-labeled neurons were found in the auditory cortex (AC), the dorsal nucleus of the lateral lemniscus (DNLL), the nucleus reticularis gigantocellularis pars ventralis (RGcv), and the dorsal column nuclei (DColN) and the spinal trigeminal complex (TrS). These data suggest that two patterns of innervation are seen for afferent fibers from regions with bilateral connections to the IC. The first pattern, typified by projections from AC, DNLL, RGcv, the DColN and TrS, primarily consists of neurons with unilaterally directed axons, extending to either the ipsilateral or contralateral IC. The second pattern, typified by projections from LSO and MSO, displays a great number of neurons whose axons apparently innervate both inferior colliculi, presumably through a process of axon collateralization. The bilateral projection of axons from individual neurons in these two nuclei possibly reflects their involvement in the processing of sensory information from the two cochleas and may represent at least one pathway whereby binaural information is relayed to both inferior colliculi.

Animals↗

Inhibition has little effect on response latencies in the inferior colliculus.

The inferior colliculi of all mammals are characterized by a wide range of first-spike response latencies that can greatly exceed the minimum time required for the transmission of input through the lower brainstem. The mechanisms that account for long response latencies of up to 50 ms are unclear, but one hypothesis is that an early inhibition plays a role in shaping latency. To test this hypothesis, response latencies were measured in the inferior colliculi of the pallid and mustached bats before and during the blockade of GABAa and glycine receptors. The effect of blocking inhibition on response latency was compared under stimulus conditions that produced the shortest latency in the predrug condition. Multibarrel "piggyback" electrodes were used to iontophoretically apply bicuculline and strychnine sequentially while recording from single neurons. Predrug latencies ranged from 9 to 26 ms in the pallid bat and from 4 to 17 ms in the mustached bat. Despite large increases in response magnitude and response duration following disinhibition, the blockade of inhibitory receptors had modest effects on response latency. In the pallid bat, blocking GABA receptors produced latency changes that ranged from -3.8 to +0.2 ms, while blocking glycine receptors produced changes from -0.1 to +1.7 ms. Similarly, in the mustached bat, blocking GABA receptors caused changes ranging from -10.3 to +1.4 ms; blocking glycine receptors in the mustached bat caused changes from -3.6 to +1.0 ms. The large change of -10.3 ms was an exception. In both species, the majority of neurons showed changes of <1 ms. We conclude that a fast, early inhibitory input does not appear to play a significant role in shaping the wide range of response latencies present in the inferior colliculi of mustached and pallid bats.

Acepromazine↗

Sensorineural hearing loss and word deafness caused by a mesencephalic lesion: clinicoelectrophysiologic correlations.

OBJECTIVE: To assess the role of inferior colliculi as a generator of Wave V of brainstem auditory evoked potentials and in modulating the olivocochlear efferent auditory system. STUDY DESIGN: Case review. SETTING: University and tertiary referral centers. PATIENTS: Case report of a patient with word deafness caused by mesencephalic hemorrhage according to audiologic and electrophysiologic findings. RESULTS: The patient is a 48-year-old woman who suffered word deafness caused by hemorrhage localized at the quadrigeminal plate (including the inferior colliculi). At a follow-up visit, her pure-tone audiogram revealed symmetric severe sensorineural hearing loss that had partially resolved, whereas speech audiometry showed persistent word deafness. Acoustic reflexes were elicited, with normal thresholds bilaterally. Transient evoked otoacoustic emissions were recorded from both ears, with normal response and signal-to-noise ratio, but there was a failure for their amplitude to be suppressed with contralateral sound stimulation. Brainstem auditory evoked potentials were of normal amplitude and latencies bilaterally. CONCLUSION: The finding of normal brainstem auditory evoked potentials supports the view that the neural generator of Wave V lies caudally to the inferior colliculi. Moreover, the abnormal suppression of transient evoked otoacoustic emissions indicates that descending collicular input is capable of modulating levels of excitability within the olivary nucleus and the cochlea.

Audiometry, Pure-Tone↗

The effect of 1,3-dinitrobenzene on the functioning of the auditory pathway in the rat.

1,3-Dinitrobenzene (DNB) has previously been shown to be neuropathic, causing gliovascular lesioning in the rat brainstem, with the nuclei of the auditory pathway being particularly affected. Lesion severity was shown to be dependent on functional activity, which could be markedly decreased within one pathway by monaurally reducing sensory input. The aim of this study was to characterise the changes in electrophysiological and vascular function associated with this asymmetric lesioning. Depth electrodes located in the inferior colliculi were used to measure wave II and IV of the auditory evoked response (AER) and collicular blood flow. These were measured up to eight days after DNB exposure in rats, in which preexisting reduction in sensory input in one ear was achieved by tympanic membrane rupture. Significant increases of between 14-27 dB were seen in the mean stimulus level required to generate a 50% isoamplitude response for wave IV in the intact (ie vulnerable) pathway over days 1-8 post DNB. No significant changes in this response for the other AER waves were seen over the same recording period. Significant increases in blood flow were seen in the inferior colliculi up to 24 hours after the final dose of DNB. Differences in increased flow between the colliculi were also highly significant, with peak increases of 200% and 80% seen in the intact and protected sides respectively. This difference shows that DNB enhanced blood flow appears to reflect the severity of the DNB induced functional deficit. In both cases, disturbance to normal glial function in maintaining K+ homeostasis, may underlie the neurophysiological deficit and the increase in blood flow seen at the level of the inferior colliculi. These asymmetric functional changes were also parallelled by the differential lesion severity between the protected and unprotected pathways. Hence, protection against DNB glial lesion severity by reduction in sensory input, and consequently metabolic demand, is paralleled by the early vascular response and functional neuronal deficit seen over the eight day post DNB recording period.

Acoustic Stimulation↗

Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus.

The superior olivary complex is a major source of auditory projections to the inferior colliculus. Although the projections from the medial and lateral superior olivary nuclei have been well characterized, projections from the surrounding periolivary nuclei have received relatively little attention. In the guinea pig, cytoarchitectonic criteria can be used to distinguish 11 periolivary nuclei that can be divided into four groups. These are: 1) a lateral group that comprises the anterolateral and posteroventral periolivary nuclei and the lateral nucleus of the trapezoid body; 2) a dorsal group that comprises the dorsal and dorsolateral periolivary nuclei; 3) a ventral group that comprises the rostral, ventromedial, and anteroventral periolivary nuclei and the ventral nucleus of the trapezoid body; and 4) a medial group that comprises the superior paraolivary nucleus and the medial nucleus of the trapezoid body. In the present study we used horseradish peroxidase and fluorescent tracers to identify olivocollicular cells in each of the periolivary nuclei. The lateral, dorsal, and medial periolivary groups project bilaterally, and the ventral periolivary group projects ipsilaterally. Within groups, individual nuclei contain different numbers of olivocollicular cells. The posteroventral periolivary nucleus is the only periolivary nucleus that does not project to the inferior colliculus. The superior paraolivary nucleus is the only periolivary nucleus that contains significant numbers of individual cells that project to both inferior colliculi. The remaining periolivary nuclei project only ipsilaterally or contain separate populations of cells that project to the two inferior colliculi.

Animals↗

Traumatic brainstem deafness with normal brainstem auditory evoked potentials.

A 48-year-old woman became totally deaf after a head injury. Magnetic resonance imaging showed bilateral contusions around the inferior colliculi and the brainstem auditory evoked potentials (BAEP) failed to show any abnormality. This case demonstrates that small, symmetrical, bilateral lesions around the inferior colliculi may cause deafness and may still be associated with a normal BAEP.

Auditory Pathways↗

Glutamic acid decarboxylase-containing neurons in the dorsal column nuclei of the cat.

The retrograde transport of horseradish peroxidase (HRP) and immunocytochemistry for glutamic acid decarboxylase (GAD) have been employed to examine whether local circuit neurons (LCNs) exist in the dorsal column nuclei (DCN) and whether these neurons may be GABA-ergic. Observations focused on the dorsal part of the middle cuneate nucleus (MCd), since this region has been previously shown to contain projecting neurons whose axons terminate almost exclusively in the contralateral thalamus. After large injections of HRP in the nucleus ventralis posterolateralis and surrounding structures of the feline thalamus, the majority of neurons in MCd are labeled. These represent about 89% of the neurons in MCd as counted in 40-microns frozen sections, and about 69% as counted in plastic-embedded, 2.5-microns-thick section. Unlabeled by the same injections are some medium to large neurons at the dorsal rim of MCd, and many characteristically small (mean = +/- 250 microns2) neurons at the periphery of the cell clusters formed by thalamic-projecting neurons. These small neurons represent 10-12% of the neuronal population of MCd, as counted in 40-microns-thick frozen sections, and about 30%, as counted in plastic-embedded, 2.5-microns-thick sections. Neurons in this size range are also unlabeled after injection of retrograde tracer in the pretectal area, inferior and superior colliculi, inferior olivary complex, and/or spinal cord. These injections, however, result in the labeling of neurons along the dorsal rim of MCd and/or in other regions of the cuneate nucleus. In adult, colchicine-treated cats, the use of anti-GAD serum reveals a population of labeled neurons uniformly distributed throughout the DCN. In MCd, these are small (mean = +/- 235 microns2) neurons mainly intercalated between cell clusters, and represent about 25% of the neuronal population of this nuclear subdivision as counted in plastic-embedded, 2.5-microns-thick sections. Labeled processes densely infiltrate the cell clusters, and labeled varicosities appear to cover the soma and dendrites of unlabeled neurons. At the electron-microscopic level, most labeled profiles contain vesicles and correspond to F boutons usually involved in "axoaxonic" contacts with terminals of dorsal root afferent and presynaptic to dendrites. Other vesicle-containing, GAD-positive endings seem to correspond to the P boutons described by Ellis and Rustioni (1981) and are believed to be, at least in part, of dendritic origin. It is suggested that GAD-positive neurons are GABA-ergic LCNs and that these can mediate both pre- and postsynaptic inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

MR imaging of the mesencephalic tectum: normal and pathologic variations.

Variations of the quadrigeminal plate (mesencephalic tectum) were determined on midline sagittal MR images of the brain in 93 patients without known mesencephalic abnormalities and in 10 patients with known aqueductal stenosis or obstruction. Measurements of the thicknesses of the superior and inferior colliculi and the length of the tectum were made on the midline sagittal section. Images were obtained with a 0.5 T system with spin-echo pulse sequences using a TE of 30 or 40 msec with a TR of 500-1500 msec. The average thickness of the superior and inferior colliculi was about 5 mm, but the range was from 2-7 mm on the midline sagittal section. Abnormally thin colliculi appeared to have no clinical significance while abnormal thickness was observed in patients with neoplastic disease, sarcoidosis, and mesencephalic "beaking." While most neoplasms have abnormal signal intensity on T2-weighted images, small lesions may be difficult to perceive on transaxial images due to volume averaging or noncontiguous sections. Measurements of the tectum, on the commonly obtained midline sagittal section, may be useful for patients with small infiltrative lesions.

Adolescent↗

[Characteristics of borderline modulation frequencies in the differentiation of tonal and amplitude-modulated stimuli following the removal of the inferior colliculus in rats].

Elaboration of differentiation between sound stimuli was carried out in 15 laboratory rats. After bilateral ablations of auditory inferior colliculi the border frequency of stimulus amplitude modulation was determined for all rats when they still could differentiate between tonal and amplitude-modulated stimuli. Decrease in frequency of modulation by 2 Hz and more from the border frequency caused a complete loss of ability to differentiate. In all rats bilateral inferior colliculi ablations completely disturbed differentiation between tonal and amplitude-modulated signals with modulation frequency below 183-191 Hz (the range of border frequencies). The surgery however did not affect differentiation between tonal and amplitude-modulated signals with the modulation frequencies above 183-191 Hz. The data suggest that the functions of completion of coding of amplitude-modulated stimuli in the auditory system is strictly linked with definite structures.

Acoustic Stimulation↗

Central deafness associated with a midbrain lesion.

Central deafness has been linked historically to bihemispheric involvement of the temporal lobe, with more recent findings suggesting that compromise of other cortical and subcortical structures can also result in this disorder. The present investigation extends our understanding of the potential anatomical correlates to central deafness by demonstrating that bilateral involvement of an auditory structure within the midbrain can additionally result in this condition. Our subject was a 21-year-old male with a subarachnoid bleed affecting both inferior colliculi. Significant auditory deficits were noted for the middle and late auditory evoked potentials, while electrophysiologic measures of the periphery indicated normal function. The patient was enrolled in a rehabilitation program for approximately 14 weeks. Although initially unresponsive to sounds, the patient regained most of his auditory abilities during the 10 months he was followed. This case documents the range of auditory deficits that may be associated with damage to the inferior colliculi, and it profiles a hierarchical recovery of auditory function consistent with test findings.

Adult↗

A monotonic code for sound azimuth in primate inferior colliculus.

We investigated the format of the code for sound location in the inferior colliculi of three awake monkeys (Macaca mulatta). We found that roughly half of our sample of 99 neurons was sensitive to the free-field locations of broadband noise presented in the frontal hemisphere. Such neurons nearly always responded monotonically as a function of sound azimuth, with stronger responses for more contralateral sound locations. Few, if any, neurons had circumscribed receptive fields. Spatial sensitivity was broad: the proportion of the total sample of neurons responding to a sound at a given location ranged from 30% for ipsilateral locations to 80% for contralateral locations. These findings suggest that sound azimuth is represented via a population rate code of very broadly responsive neurons in primate inferior colliculi. This representation differs in format from the place code used for encoding the locations of visual and tactile stimuli and poses problems for the eventual convergence of auditory and visual or somatosensory signals. Accordingly, models for converting this representation into a place code are discussed.

Acoustic Stimulation↗

Vascular factors in the neurotoxic damage caused by 1,3-dinitrobenzene in the rat.

Using a 3 x 10 mg/kg dose schedule of 1,3-dinitrobenzene (DNB) over two days in Fischer rats, we have found the following changes in vascular function and structure during the early phase of the symmetrical brain stem lesions. 1. Marked increase in cerebral blood flow generally but especially in the inferior colliculi, from 6 h after the final dose of DNB. 2. Increasing incidence of petechial haemorrhages in inferior colliculi, cerebellar roof, vestibular and superior olivary nuclei from 12 h. 3. Focal leakage of horseradish peroxidase and many sleeve-like arteriolar haemorrhages seen in vibratome sections and by scanning electron microscopy (SEM) in these regions from 12 h. 4. Periarteriolar oedema and protein leakage present in step-serial sections in these regions from 12 h, with astrocyte swelling and occasional small infarcts. These changes suggest that the vascular bed may play an important role in the pathogenesis of these lesions, perhaps in parallel with early astroglial damage. They are discussed in relation to (i) the known presence of xanthine oxidase in the vascular bed of the brain and the likelihood of "useless redox cycling' with free radical generation from this enzyme's interaction with nitroheterocyclic compounds, and (ii) the possible role of free radical damage to endothelial cells in this intoxication and in the analogous lesions of natural and experimental Wernicke's encephalopathy.

Animals↗