Sound-evoked activity in primary afferent neurons of a mammalian vestibular system.

HYPOTHESIS: Some primary vestibular afferents in the cat respond to sound at moderately intense sound levels. BACKGROUND: In fish and amphibians, parts of the vestibular apparatus are involved in audition. The possibility was explored that the vestibular system in mammals is also acoustically responsive. METHODS: Microelectrodes were used to record from single afferent fibers in the inferior vestibular nerve of the cat; some acoustically responsive fibers were labeled intracellularly with biocytin. RESULTS: Vestibular afferents with regular spontaneous activity were unresponsive to sound, whereas a sizable fraction of vestibular afferents with irregular activity were acoustically responsive. Labeling experiments demonstrated that acoustically responsive afferents innervate the saccule, have cell bodies in Scarpa's ganglion, and project to central regions both inside and outside the traditional boundaries of the vestibular nuclei. Acoustically responsive vestibular afferents responded to sound with shorter latencies than cochlear afferents but had higher thresholds (> 90 dB sound pressure level) and responded only in the range 0.1-3.0 kHz. In contrast to cochlear afferents, efferent stimulation excited background activity and proportionately increased sound-evoked responses in these vestibular afferents, that is, there was centrally mediated enhancement of gain (gain = spike-rate/motion). CONCLUSIONS: The evolutionary conservation of a saccular auditory pathway in mammals suggests that it confers survival advantages. Recent evidence suggests that acoustically responsive saccular afferents trigger acoustic reflexes of the sternocleidomastoid muscle, and hence measurement of such reflexes may provide a relatively simple test for saccular dysfunction.

Spontaneous activity and frequency selectivity of acoustically responsive vestibular afferents in the cat.

1. Recordings were made from single afferent fibers in the inferior vestibular nerve. Firing rates of a substantial portion of the afferents with irregular background activity increased in response to moderately intense tone bursts. 2. Spontaneous activity from acoustically responsive vestibular afferents was statistically analyzed and compared with data from a more widespread sampling of primary afferents in the cat's vestibulocochlear nerve. Acoustically responsive vestibular afferents had interspike interval histograms with modes > 10 ms, coefficients of variation > 0.15, and skews > 0.88. On the basis of spontaneous activity, these afferents were easily distinguishable from cochlear afferents and regular vestibular afferents, but no obvious features differentiated them from other irregular vestibular afferents. 3. The distributions of spike intervals in the spontaneous activity of acoustically responsive vestibular afferents were fitted by Erlang probability density functions describing the second-order interarrival times of a Poisson process initiated after a finite delay (refractory period). 4. Acoustically responsive vestibular afferents had broad, V-shaped tuning curves with best frequencies between 500 and 1,000 Hz, thresholds of > or = 90 dB SPL, and shapes comparable with the tuning-curve "tails" of cochlear afferents. In contrast to cochlear-nerve afferents, acoustically responsive vestibular afferents did not show a strong relationship between spontaneous rate and threshold. 5. We compare the acoustic frequency selectivity of vestibular and cochlear afferents in terms of their functional and evolutionary relationships. Our data and those of others indicate that acoustically responsive vestibular afferents are likely to provide an input to the acoustic activation of the sternocleidomastoid muscle in humans, and they may provide an input to other acoustic reflexes such as the middle-ear-muscle reflexes.

Acoustically responsive fibers in the vestibular nerve of the cat.

Recordings were made from single afferent fibers in the inferior vestibular nerve, which innervates the saccule and posterior semicircular canal. A substantial portion of the fibers with irregular background activity increased their firing in response to moderately intense clicks and tones. In responsive fibers, acoustic clicks evoked action potentials with minimum latencies of < or = 1.0 msec. Fibers fell into two classes, with the shortest latency either to condensation clicks (PUSH fibers) or to rarefaction clicks (PULL fibers). Low-frequency (800 Hz) tone bursts at moderately high sound levels (> 80 dB SPL) caused synchronization of spikes to preferred phases of the tone cycle. PUSH and PULL fibers had preferred response phases approximately 180 degrees apart. These two response classes are consistent with fibers that innervate hair cells having opposite morphological polarizations, an arrangement found in the saccule. With low-frequency tone bursts, sound levels of > or = 90 dB SPL evoked increases in mean spike rate. Spike rates increased monotonically with sound level without saturating at levels < or = 115 dB SPL. Contraction of the middle-ear muscles decreased responses to sound, consistent with the sound transmission path being through the middle ear. Several fibers were labeled with biocytin and traced. All labeled fibers had bipolar cell bodies in the inferior vestibular ganglion with peripheral processes extending toward the saccular nerve and central processes in the vestibular nerve. Two fibers were traced to the saccular epithelium. One fiber was traced centrally and arborized extensively in vestibular nuclei and a region ventromedial to the cochlear nucleus. Our results confirm and extend previous suggestions that the mammalian saccule responds to sound at frequencies and levels within the normal range of human hearing. We suggest a number of auditory roles that these fibers may play in the everyday life of mammals.

Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat.

In the preceding article (McCue and Guinan, 1994) we described a class of vestibular primary afferent fibers in the cat that responds vigorously to sounds at moderately high sound levels. Like their cochlear homologs, vestibular afferents and their associated hair cells receive efferent projections from brainstem neurons. In this report, we explore efferent influences on the background activity and tone-burst responses of the acoustically responsive vestibular afferents. Shock-burst stimulation of efferents excited acoustically responsive vestibular afferents; no inhibition was seen. A fast excitatory component built up within 100-200 msec of shock-burst onset and decayed with a similar time course at the end of each shock burst. During repeated 400 msec shock bursts at 1.5 sec intervals, a slow excitatory component grew over 20-40 sec and then decayed, even though the shock bursts continued. Efferent stimulation excited acoustically responsive vestibular afferents without appreciably changing an afferent's sound threshold or its average sound-evoked response. This evidence supports the hypothesis that excitation is due to efferent synapses on afferent fibers rather than on hair cells. Efferent stimulation enhanced the within-cycle modulation of afferent discharges evoked by a tone; that is, it increased the "AC gain." No appreciable change was noted in the degree of phase locking to low-frequency tones as measured by the synchronization index. Little or no improvement in the bidirectionality (linearity) of transduction was seen. Vestibular afferent responses to tones normally had one peak per cycle; however, during efferent stimulation, two peaks per cycle were sometimes seen. We hypothesize that this is caused by two driving components acting at different sound phases with the components differentially affected by efferent activity. We discuss the relationship of our findings to efferent influences on acoustic responses in cochlear afferent fibers. The acoustically responsive vestibular afferents provide a mammalian model for studying purely excitatory efferent effects in a hair cell system.

Primary T-cell lymphoma of the brainstem.

Most primary CNS lymphomas are non-Hodgkin's lymphomas of B-cell lineage. We report a case of a small lymphocytic-type T-cell lymphoma localized primarily to the brainstem and compare the characteristics of primary CNS T-cell lymphomas with those of primary CNS B-cell lymphomas.

Anatomical and functional segregation in the stapedius motoneuron pool of the cat.

1. Electromyographic activity (EMG) is detectable in the feline stapedius muscle 6-10 ms after the onset of an intense sound presented to either ear. Stapedius reflexes evoked by ipsilateral and contralateral sound were measured electromyographically before and after brain stem lesions were made. In some cases, stapedius motor axons were cut; in others, brain stem regions containing motoneuron cell bodies were destroyed electrolytically. 2. Electrolytic lesions that contacted an anatomically separate cluster of stapedius motoneurons (the ventromedial perifacial group) greatly reduced responses to contralateral sound without noticeably affecting responses to ipsilateral sound. 3. Electrolytic lesions in other brain stem areas had different effects; one appeared to reduce responses to ipsilateral sound selectively, whereas others reduced both responses or had little effect. 4. After subsets of stapedius motor axons were cut at the facial colliculus in the floor of the fourth ventricle, responses to contralateral sound were almost eliminated, while substantial responses to ipsilateral sound remained. 5. The results are consistent with the hypothesis that inputs from the two cochleas are distributed inhomogeneously across the stapedius motoneuron pool in such a way as to produce a segregation of function, with motoneurons in one brain stem region responding preferentially (or exclusively) to contralateral sound and motoneurons in other regions responding preferentially (or exclusively) to ipsilateral sound. This topographic organization of acoustic input to the stapedius motoneuron pool produces a "central partitioning" in the acoustic stapedius reflexes similar in some respects to the partitioning observed in proprioceptive spinal reflexes.

Asymmetries in the acoustic reflexes of the cat stapedius muscle.

Electromyographic activity (EMG) was used to monitor contractions of the stapedius muscle evoked by both ipsilateral and contralateral sound in ketamine-anesthetized or decerebrate cats. After the onset of a continuing tone, stapedius EMG often had bursts of activity at regular intervals; similar bursts were also observed in the EMG from the tensor tympani muscle. Plots of the r.m.s. amplitude of stapedius-EMG versus sound level usually had a steep rising phase (small dynamic range) and a plateau at high sound levels. For sound stimulation at 1 kHz, the crossed stapedius reflex had a lower maximum amplitude (ave. amplitude ratio: 0.37) and a higher threshold (ave. 8 dB) than the uncrossed reflex. Since the uncrossed reflex evokes considerably more stapedius EMG than does the crossed reflex, it probably produces correspondingly greater changes in middle-ear sound transmission.

Behaviour of human motor units in different muscles during linearly varying contractions.

1. The electrical activity of up to eight concurrently active motor units has been recorded from the human deltoid and first dorsal interosseous (f.d.i.) muscles. The detected myoelectric signals have been decomposed into their constituent motor-unit action potential trains using a recently developed technique.2. Concurrently active motor unit behaviour has been examined during triangular force-varying isometric contractions reaching 40 and 80% of maximal voluntary contraction (m.v.c.). Experiments were performed on four normal subjects and three groups of highly trained performers (long-distance swimmers, powerlifters and pianists).3. Results revealed a highly ordered recruitment and decruitment scheme, based on motoneurone excitability, in both muscles and in all subject groups.4. Differences were observed between the initial (recruitment) and final (decruitment) firing rates in each muscle. These parameters were invariant with respect to the force rates studied, although some differences were observed among subject groups.5. In general, firing rates of f.d.i. motor units increased steadily with increasing force (up to 80% m.v.c.). The firing rates of deltoid motor units rose sharply just after recruitment and then increased only slightly thereafter.6. Recruitment was found to be the major mechanism for generating extra force between 40 and 80% m.v.c. in the deltoid, while rate coding played the major role in the f.d.i.7. The potential of rate coding for increasing force levels up to m.v.c. is discussed.

Control scheme governing concurrently active human motor units during voluntary contractions.

1. The electrical activity of up to eight concurrently active motor units has been recorded from the human deltoid and first dorsal interosseous muscles. The resulting composite myoelectric signals have been decomposed into their constituent motor-unit action potential trains using a recently developed technique.2. A computer cross-correlation analysis has been performed on motor-unit firing rate and muscle-force output records obtained from both constant-force and triangular force-varying isometric contractions performed by normal subjects, and three groups of highly trained performers (long-distance swimmers, powerlifters and pianists).3. The temporal relationships between firing rate activity and force output have provided evidence that the deltoid of long-distance swimmers has a significantly higher percentage of slowly fatiguing fibres than that of normal subjects.4. Results showed that both muscles are incapable of producing a purely isotonic contraction under isometric conditions. Small, possibly compensatory force variations at 1-2 Hz result from a common drive to all active motoneurones in a single muscle pool.5. Rapid force reversals during triangular, force-varying isometric contractions appear to be accomplished through a size-related motor-unit control scheme. All firing rates decline prior to the force peak, but small motor units with slow-twitch responses tend to decrease their firing rates before large, fast-twitch motor units. This mechanism is not visually controlled, and does not depend on force rate in non-ballistic contractions.