Oscillatory discharges in the auditory midbrain of the big brown bat contribute to coding of echo delay.

Subsequent to his breakthrough discovery of delay-tuned neurons in the bat's auditory midbrain and cortex, Albert Feng proposed that neural computations for echo delay involve intrinsic oscillatory discharges generated in the inferior colliculus (IC). To explore further the presence of these neural oscillations, we recorded multiple unit activity with a novel annular low impedance electrode from the IC of anesthetized big brown bats and Seba's short-tailed fruit bats. In both species, responses to tones, noise bursts, and FM sweeps contain long latency components, extending up to 60 ms post-stimulus onset, organized in periodic, oscillatory-like patterns at frequencies of 360-740 Hz. Latencies of this oscillatory activity resemble the wide distributions of single neuron response latencies in the IC. In big brown bats, oscillations lasting up to 30 ms after pulse onset emerge in response to single FM pulse-echo pairs, at particular pulse-echo delays. Oscillatory responses to pulses and evoked responses to echoes overlap extensively at short echo delays (5-7 ms), creating interference-like patterns. At longer echo delays, responses are separately evident to both pulses and echoes, with less overlap. These results extend Feng's reports of IC oscillations, and point to different processing mechanisms underlying perception of short vs long echo delays.

Gayet-Wernicke Syndrome: The eye surgeon in a French neurologic eponym.

Gayet-Wernicke syndrome is an eponym mainly used in France. In this article, we revisit Charles Gayet's (1833-1904) speciality and his patient example that gave rise to the eponym. Charles Gayet attributed the anatomical lesions to inflammation. However, they were mainly due to hemorrhage, as Wernicke's term "polioencéphalite supérieure aiguë hémorragique" (polio-encephalitis superior haemorrhagica) explicitly indicates. The pathology of Gayet's case did not involve the mamillary bodies, colliculi, or cerebellum. Gayet did not mention abnormal memory functions, which are also cardinal signs of Wernicke-Korsakoff's disease. We argue that the Gayet-Wernicke eponym is not merited and that the more common international term "Wernicke-Korsakoff syndrome" should be used in France as elsewhere in the world.

Reversible Hearing Impairment Due to Inferior Colliculi Compression by a Pineal Glial Cyst.

Pineal glial cysts associated with bilateral hearing impairment are very rare. Here, we present the case of a 13-year-old boy with a pineal cyst, which caused severe bilateral hearing impairment persisting from 6 years of age. When the patient was 6 years old, the bilateral hearing acuity was about 40 dB on audiometry. Upon admission to our otolaryngology department, his audiogram revealed a bilateral worsening of the hearing acuity (80 dB). Magnetic resonance imaging (MRI) revealed an abnormal pineal cyst with tectal compression from the left with hardly normal bilateral brainstem auditory evoked potentials (BAEPs). We obtained informed consent for exploratory surgery and employed the right occipital transtentorial approach for pineal cyst removal. Based on histological examination, we diagnosed a glial cyst of the pineal gland. At 12 months postoperatively, the patient's hearing improved, showing a bilateral hearing acuity of 40 dB on audiometry. Since the auditory pathway has both crossed and uncrossed fibers at the upper pons and midbrain level, compression at the lateral lemniscus or inferior colliculus level can cause bilateral hearing impairment. In the present case, there was a possible slow pineal cyst growth that eventually compressed the upper pons to the midbrain, lateral lemniscuses, or inferior colliculi from the left side, this eventually led to bilateral hearing impairment. These findings indicate that surgery can improve hearing acuity in patients with a pineal cyst associated with progressive hearing impairment.

Demonstration of Microsurgical Technique and Nuances for the Resection of a Midbrain Tectal Glioma via the Transcollicular Approach: 3-Dimensional Operative Video.

Tectal gliomas are a rare subset of intrinsic brainstem lesions. The microsurgical resection of these lesions remains a major challenge.1,2 Transcollicular approaches on one side, via the superior or inferior colliculi or both, are neurologically well tolerated without obvious or major auditory or oculomotor consequences. However, any postoperative acute visually triggered saccadic abnormalities caused by iatrogenic superior colliculus damage generally resolve during the postoperative period, as other oculomotor structures compensate for these functions in unilateral lesions. In this surgical video, we present a 37-yr-old man with long-standing seizures, new onset headaches, progressive ataxic gait, and imbalance. Magnetic resonance imaging (MRI) showed a circumscribed nonenhancing dorsal midbrain cystic mass with compression on the aqueduct causing hydrocephalus. The lesion had a low signal intensity on T1-weighted images and a high signal intensity on T2-weighted images. The patient first underwent an endoscopic third ventriculostomy. Although his headaches greatly improved after the third ventriculostomy, he remained quite symptomatic in terms of gait imbalance and ataxia. The patient underwent a supracerebellar, infratentorial, transcollicular approach for resection of the tectal tumor. Simultaneously, motor and somatosensory evoked potentials were monitored. Both the surgery and the postoperative course were uneventful, with postoperative MRI showing gross total resection of the mass, and histopathology indicating a WHO (World Health Organization) grade I pilocytic astrocytoma. The patient continued to do well without recurrence at 2-yr follow-up. In this video, we demonstrate step-by-step microsurgical techniques for resecting these challenging tectal gliomas via the infratentorial-supracerebellar-transcollicular approach. The patient consented to the procedure and publication of his images.

Sensory systems in birds: What we have learned from studying sensory specialists.

"Diversity" is an apt descriptor of the research career of Jack Pettigrew as it ranged from the study of trees, to clinical conditions, to sensory neuroscience. Within sensory neuroscience, he was fascinated by the evolution of sensory systems across species. Here, we review some of his work on avian sensory specialists and research that he inspired in others. We begin with an overview of the importance of the Wulst in stereopsis and the need for further study of the Wulst in relation to binocularity across avian species. Next, we summarize recent anatomical, behavioral, and physiological studies on optic flow specializations in hummingbirds. Beyond vision, we discuss the first evidence of a tactile "fovea" in birds and how this led to detailed studies of tactile specializations in waterfowl and sensorimotor systems in parrots. We then describe preliminary studies by Pettigrew of two endemic Australian species, the plains-wanderer (Pedionomus torquatus) and letter-winged kite (Elanus scriptus), that suggest the evolution of some unique auditory and visual specializations in relation to their unique behavior and ecology. Finally, we conclude by emphasizing the importance of a comparative and integrative approach to understanding avian sensory systems and provide an example of one system that has yet to be properly examined: tactile facial bristles in birds. Through reviewing this research and offering future avenues for discovery, we hope that others also embrace the comparative approach to understanding sensory system evolution in birds and other vertebrates.

[A case of Wernicke encephalopathy with hypoacusia and MR high intensity of the inferior colliculi that normalized after thiamine administration].

A 61-year-old man was admitted to our institution with progressive hypoacusia, double vision, and lightheadedness. Neurological examination on day 6 of his illness showed severe hypoacusia, mild confusion, ocular motility disorder, truncal ataxia and absence of a deep tendon reflex. MRI fluid-attenuated inversion recovery imaging revealed symmetrical high intensities in the tectum of the midbrain, involving the bilateral inferior colliculi and the bilateral medial thalami, which suggested Wernicke encephalopathy (WE). Thiamine was administered immediately after completion of the MRI, and the patients' hearing and other abnormal neurologic signs improved rapidly within a few days, except for the absence of the deep tendon reflex. Whole blood examination at admission revealed very low levels of vitamin B1. The patient was discharged on day 19, and MRI on day 39 showed the disappearance of the abnormal high intensities involving the bilateral inferior colliculi. The present case indicates that hypoacusia and abnormal MRI signal due to WE might be normalized by administration of thiamine a few days after the onset of symptoms.

The auditory corticocollicular system: molecular and circuit-level considerations.

We live in a world imbued with a rich mixture of complex sounds. Successful acoustic communication requires the ability to extract meaning from those sounds, even when degraded. One strategy used by the auditory system is to harness high-level contextual cues to modulate the perception of incoming sounds. An ideal substrate for this process is the massive set of top-down projections emanating from virtually every level of the auditory system. In this review, we provide a molecular and circuit-level description of one of the largest of these pathways: the auditory corticocollicular pathway. While its functional role remains to be fully elucidated, activation of this projection system can rapidly and profoundly change the tuning of neurons in the inferior colliculus. Several specific issues are reviewed. First, we describe the complex heterogeneous anatomical organization of the corticocollicular pathway, with particular emphasis on the topography of the pathway. We also review the laminar origin of the corticocollicular projection and discuss known physiological and morphological differences between subsets of corticocollicular cells. Finally, we discuss recent findings about the molecular micro-organization of the inferior colliculus and how it interfaces with corticocollicular termination patterns. Given the assortment of molecular tools now available to the investigator, it is hoped that his review will help guide future research on the role of this pathway in normal hearing.

Gómez-López-Hernández syndrome in a child born to consanguineous parents: new evidence for an autosomal-recessive pattern of inheritance?

BACKGROUND: Gómez-López-Hernández syndrome is a rare genetic disease characterized by scalp alopecia with trigeminal anesthesia, brachycephaly or turribrachycephaly, midface retrusion, and rhombencephalosynapsis. We report the second case with this condition who presented with consanguineous parents. PATIENT: This boy was evaluated shortly after birth because of suspected craniosynostosis. He was the only son of healthy, consanguineous parents (his maternal grandmother and his paternal great-grandfather were siblings). His examination was notable for turribrachycephaly, prominent forehead, bilateral parietotemporal alopecia, midfacial retrusion, anteverted nostrils, micrognathia, low-set and posteriorly rotated ears, and short neck with redundant skin. Radiographs and tridimensional computed tomography scan of skull revealed lambdoid craniosynostosis. Brain magnetic resonance imaging revealed complete rhombencephalosynapsis, aqueductal stenosis, fused colliculi, abnormal superior cerebellar penducle, mild ventriculomegaly, and dysgenesis of the corpus callosum. CONCLUSIONS: Since its first description, 34 patients with this condition have been reported. The etiology of Gómez-López-Hernández syndrome is unknown. However, it is noteworthy that the patient in this report presented with a family history of consanguinity because this finding reinforces the possibility of an autosomal-recessive inheritance for this condition.

Arm movements induced by electrical microstimulation in the superior colliculus of the macaque monkey.

Neuronal activity in the deep layers of the macaque (Macaca mulatta) superior colliculus (SC) and the underlying reticular formation is correlated with the initiation and execution of arm movements (Werner, 1993). Although the correlation of this activity with EMGs of proximal arm muscles is as strong as in motor cortex (Werner et al., 1997a; Stuphorn et al., 1999), little is known about the influence of electrical microstimulation in the SC on the initiation and trajectories of arm movements. Our experiments on three macaque monkeys clearly show that arm movements can be elicited by electrical microstimulation in the deep layers of the lateral SC and underlying reticular formation. The most extensively trained monkey, M1, extended his arm toward the screen in front of him more or less stereotypically upon electrical SC stimulation. In two other monkeys, M2 and M3, a larger repertoire of arm movements were elicited, categorized into three movement types, and compared before (M3) and after (M2 and M3) training: twitch (56% vs. 62%), lift (6% vs. 5%), and extend (37% vs. 32%), respectively. Therefore, arm movements induced by electrical stimulation in the monkey SC represent a further component of the functional repertoire of the SC using its impact on motoneurons in the spinal cord, probably via premotor neurons in the brainstem, as well as on structures involved in executing more complex movements such as target-directed reaching. Therefore, the macaque SC could be involved directly in the initiation, execution, and amendment of arm and hand movements.

Transient tonic upgaze deviation: a neuro-ophthalmological complication of acute cerebellitis.

Acute cerebellitis in children is an inflammatory syndrome with symptoms of cerebellar dysfunction. We describe a 3-year-old boy with acute cerebellitis who had cerebellar tonsillar herniation, hydrocephalus, and transient tonic bilateral upward gaze deviation. Although no etiology for his acute cerebellitis was determined, he fully recovered with high-dose corticosteroids, intravenous immunoglobulin, and antimicrobial therapy. We propose that there was tonic irritation of the upward gaze generator cells in the superior colliculus as an explanation for temporary disturbance of his ocular gaze.

Metronidazole-induced encephalopathy in a patient with end-stage liver disease.

Purpose. Metronidazole-induced encephalopathy (MIE) has been rarely reported. We report a case in a patient with end-stage liver disease (ESLD). Summary. A 63-year-old male with ESLD secondary to hepatitis C virus presented with progressively worsening fatigue, slurred speech, aphasia, vomiting, and left-sided facial droop after completing a 2-week course of metronidazole for recurrent Clostridium difficile-associated diarrhea. He completed a previous course of metronidazole 3 weeks prior to presentation. He is on the liver transplant waiting list and has known hepatic encephalopathy. MRI revealed hyperintense T2 signals involving the bilateral dentate nuclei, inferior colliculi and splenium of the corpus callosum, and increased diffusion restriction at the splenium of the corpus callosum. His neurological function improved over the next several days. He underwent liver transplantation 6 days after admission. A follow-up MRI 6 weeks after presentation revealed resolution of abnormalities; however, paresthesias persisted 6 months after MIE diagnosis. Conclusion. An ESLD patient with hepatic encephalopathy developed MIE after a relatively short course of metronidazole. Metronidazole has been shown to accumulate in patients with ESLD. Increased awareness for neurotoxicity when using metronidazole in ESLD patients is warranted, especially in those with potentially confounding hepatic encephalopathy.

[The significance of stress: its role in the auditory system and the pathogenesis of tinnitus]. / Bedeutung von Stress : Seine Rolle im auditorischen System und bei der Tinnitusentstehung.

Emotional stress is often associated with auditory phenomena such as hyperacusis, tinnitus, Ménière's disease and vertigo. Stress develops as a result of a person's attempts to come to terms with the increased or unexpected demands of his or her environment. Stress serves to protect one from physical danger and to temporarily increase one's performance in order to increase the probability of survival. Sleep and appetite are particularly reduced, while anxiety increases. The mental changes induced by stress may contribute to the onset or exacerbation of tinnitus. The following links exist between the auditory and stress systems: the limbic system, which regulates instinctive behavior and emotions, is linked to the auditory system via the medial geniculate body (amygdala). The hypothalamus, which is the integrative center of the endocrine and autonomic systems, is linked to the auditory system via the inferior colliculus. The reticular system, which is focused on the behavior pattern of attention and excitement, projects serotonergic fibers to all pathways of the auditory system, ranging from the cochlea to the auditory cortex.

Collicular vision guides nonconscious behavior.

Following destruction or deafferentation of primary visual cortex (area V1, striate cortex), clinical blindness ensues, but residual visual functions may, nevertheless, persist without perceptual consciousness (a condition termed blindsight). The study of patients with such lesions thus offers a unique opportunity to investigate what visual capacities are mediated by the extrastriate pathways that bypass V1. Here we provide evidence for a crucial role of the collicular-extrastriate pathway in nonconscious visuomotor integration by showing that, in the absence of V1, the superior colliculus (SC) is essential to translate visual signals that cannot be consciously perceived into motor outputs. We found that a gray stimulus presented in the blind field of a patient with unilateral V1 loss, although not consciously seen, can influence his behavioral and pupillary responses to consciously perceived stimuli in the intact field (implicit bilateral summation). Notably, this effect was accompanied by selective activations in the SC and in occipito-temporal extrastriate areas. However, when instead of gray stimuli we presented purple stimuli, which predominantly draw on S-cones and are thus invisible to the SC, any evidence of implicit visuomotor integration disappeared and activations in the SC dropped significantly. The present findings show that the SC acts as an interface between sensory and motor processing in the human brain, thereby providing a contribution to visually guided behavior that may remain functionally and anatomically segregated from the geniculo-striate pathway and entirely outside conscious visual experience.

The near response: the contributions of Kenji Ohtsuka, MD.

Kenji Ohtsuka, MD and his colleagues at the Sapporo Medical University have investigated the central organization of the near response with anatomical and neurophysiologic studies in cats. Based on their data and clinical observations, they proposed that the rostral pole of the superior colliculus has a critical role in the control of accommodation, vergence, and fixation. Although the central pathways have yet to be fully worked out, the contributions of Dr. Ohtsuka, who died in 2005, have laid an important foundation in the understanding of these functions.

Reward-related neuronal activity in the rat superior colliculus.

The activity of single units in the intermediate and deep layers of the superior colliculus was recorded while rats performed an operant conditioning task. On all trials, each animal pressed a bar and then inserted his snout into a food cup; on half of the trials, food reinforcement was available. To test for tactile sensitivity, on half of the trials the rats received a puff of air to the face when the snout entered the food cup. Activity of most cells was correlated with the motor activity of inserting the snout into the food cup, even when reinforcement was not available. For many cells, a larger burst of activity was seen on the reinforced trials than on trials when rats made the same movements without the presence of reward. There was no evidence that an increase in tactile sensitivity occurred when the animal retrieved the reinforcement. These results suggest that cells in the superior colliculus have an increase in activity associated with reward retrieval, which for some neurons is not dependent on simple sensory or motor factors.

Posterior cranial fossa gangliogliomas.

Ganglioglioma (GG) is an uncommon primary lesion of the central nervous system that is typically located supratentorially. There are only a few reports of GG arising from the cerebellum. To the best of our knowledge this is the first case of a cerebellar GG with supratentorial extension and a longstanding history before its recognition. In fact, this 29-year-old male presented with an 11-year history of intermittent headaches. A cranial computerized tomography (CT) performed at the onset of his complaints failed to reveal the tumor. After a particularly longstanding cephalalgic episode, the patient underwent a new CT scan that was also negative. However, magnetic resonance (MR) imaging of the brain revealed a space-occupying lesion in the right cerebellar hemisphere with extension to the level of the superior colliculi and pineal recess. The tumor was partially removed through a midline suboccipital craniotomy and supracerebellar approach. Pathological examination of the tumor showed composition of atypical ganglion cells and astrocytes, indicating the diagnosis of cerebellar GG. At last follow-up, 24 months after surgery, the patient reported a marked improvement of his clinical condition with significant reduction of intensity and frequency of the headache. The present report illustrates how cerebellar GG may remain undetectable by CT and may therefore present with a longstanding history and nonspecific signs and symptoms. MR investigation can lead to the proper diagnosis. Even after partial removal the prognosis remains good and remission of the symptoms may be achieved. In this article, we review the literature and summarize the current understanding of infratentorial GGs.

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.

Functional role of the human inferior colliculus in binaural hearing.

Psychophysical experiments were carried out in a rare case involving a 48 year old man (RJC) with a small traumatic hemorrhage of the right dorsal midbrain, including the inferior colliculus (IC). RJC had normal audiograms bilaterally, but there was a marked decrease in wave V amplitude on click-evoked brainstem auditory evoked potentials following left ear stimulation. RJC demonstrated a deficit in sound localization identification when the loudspeakers lay within the auditory hemifield contralateral to his IC lesion. Errors showed a consistent bias towards the hemifield ipsilateral to the lesion. Echo suppression was abnormally weak compared with that seen in control subjects, but only for sources contralateral to the lesion. Finally, speech intelligibility tests showed normal ability to benefit from spatial separation of target and competing speech sources. These results suggest that: (1) localizing sounds within a given hemifield relies on the integrity of the contralateral IC, (2) unilateral IC lesions give the illusion that sound sources in the 'bad' hemifield are displaced towards the 'good' hemifield, (3) the IC mediates aspects of echo suppression, and (4) lesion in the IC does not impede spatial release from masking in speech intelligibility, possibly due to that ability being more heavily mediated by cortical regions.

NMDA antagonists in the superior colliculus prevent developmental plasticity but not visual transmission or map compression.

Partial ablation of the superior colliculus (SC) at birth in hamsters compresses the retinocollicular map, increasing the amount of visual field represented at each SC location. Receptive field sizes of single SC neurons are maintained, however, preserving receptive field properties in the prelesion condition. The mechanism that allows single SC neurons to restrict the number of convergent retinal inputs and thus compensate for induced brain damage is unknown. In this study, we examined the role of N-methyl-D-aspartate (NMDA) receptors in controlling retinocollicular convergence. We found that chronic 2-amino-5-phosphonovaleric acid (APV) blockade of NMDA receptors from birth in normal hamsters resulted in enlarged single-unit receptive fields in SC neurons from normal maps and further enlargement in lesioned animals with compressed maps. The effect was linearly related to lesion size. These results suggest that NMDA receptors are necessary to control afferent/target convergence in the normal SC and to compensate for excess retinal afferents in lesioned animals. Despite the alteration in receptive field size in the APV-treated animals, a complete visual map was present in both normal and lesioned hamsters. Visual responsiveness in the treated SC was normal; thus the loss of compensatory plasticity was not due to reduced visual responsiveness. Our results argue that NMDA receptors are essential for map refinement, construction of receptive fields, and compensation for damage but not overall map compression. The results are consistent with a role for the NMDA receptor as a coincidence detector with a threshold, providing visual neurons with the ability to calculate the amount of visual space represented by competing retinal inputs through the absolute amount of coincidence in their firing patterns. This mechanism of population matching is likely to be of general importance during nervous system development.

Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field.

Patient G.Y. is able to discriminate emotional facial expressions presented in his blind (right) hemifield despite an extensive lesion of the corresponding (left) striate cortex. One proposal is that this residual ability (affective "blindsight") depends on a subcortical visual pathway comprising the superior colliculus, posterior (extrageniculate) thalamus and amygdala. Here we report differential amygdala responses in G.Y. to presentation of fearful and fear-conditioned faces in his blind (right) hemifield. These amygdala responses exhibited condition-dependent covariation with neural activity in the posterior thalamus and superior colliculus. Our results provide further evidence that an extrageniculostriate (colliculo-thalamo-amygdala) neural pathway can process fear-related stimuli independently of both the striate cortex and normal phenomenal visual awareness.