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Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons.

When cochlear pathology impairs the afferent innervation of the ventral cochlear nucleus (VCN), electrical responses of the auditory brainstem are altered and changes in cell and synaptic morphology are observed. However, the impact of deafferentation on the electrical properties of cells in the VCN is unknown. We examined the electrical properties of single neurons in the anterior and posterior VCN following bilateral cochlear removal in young rats. In control animals, two populations of cells were distinguished: those with a linear subthreshold current-voltage relationship and repetitive firing of action potentials with regular interspike intervals (type I), and those with rectifying subthreshold current-voltage relationships and phasic firing of 1-3 action potentials (type II). Measures of action potential shape further distinguished these two groups. Two weeks following cochlear removal, both electrical response patterns were still seen. Type I cells showed a higher input resistance. Deafferented single-spiking type II cells were slightly more depolarized, had smaller action potentials, smaller afterhyperpolarizations and shorter membrane time constants, whereas multiple-spiking type II cells were apparently unaffected. These changes in the electrical properties of VCN neurons following cochlear injury may adversely affect central processing of sounds presented acoustically or electrically by prostheses.

Afferent Pathways↗

Superior olivary contributions to auditory system plasticity: medial but not lateral olivocochlear neurons are the source of cochleotomy-induced GAP-43 expression in the ventral cochlear nucleus.

A unilateral cochlear lesion induces expression of the growth and plasticity-associated protein 43 (GAP-43) in fibers and their varicosities on specific types of postsynaptic profiles in the ventral cochlear nucleus (VCN), suggesting the induction of synaptic remodeling. One candidate population from which GAP-43 might emerge was neurons of the lateral olivocochlear (LOC) system residing in the lateral superior olive (LSO). Upon cochleotomy, these neurons express GAP-43 mRNA and GAP-43 protein. However, retrograde axonal tracing with Fast Blue or biotinylated dextran amine from VCN revealed that the number of 6.8 +/- 1.3 neurons in the whole ipsilateral LSO labeled in normal adult rats was distinctly small and did not rise after cochleotomy. Concluding that LOC neurons cannot be the source of GAP-43 in the VCN, we reinvestigated the pattern of GAP-43 in situ hybridization and found that, after cochleotomy, shell neurons in the regions surrounding the LSO and medial olivocochlear (MOC) neurons in the ventral nucleus of the trapezoid body up-regulated GAP-43 mRNA. We then lesioned these regions by means of stereotaxic injections of kainic acid. Destruction of shell neurons preceding an ipsilateral cochleotomy did not change the emergence of GAP-43 immunoreactivity in the VCN. However, if the contralateral MOC system was lesioned, the rise of GAP-43 immunoreactivity in VCN on the side of the cochleotomy was significantly reduced. We conclude that, after cochlear dysfunction, MOC neurons are the major (if not exclusive) source of synaptic reorganization in the VCN that could possibly entail compensatory activation of the affected ascending auditory pathway.

Animals↗

Neuronal morphology of the rabbit cochlear nucleus.

The cytoarchitecture of the cochlear nucleus in young adult albino rabbits (Cuniculus oryctolagus) has been examined in Nissl- and Golgi-impregnated material to compare rabbit cochlear nucleus with other mammalian species. Cochlear nucleus was subdivided into anteroventral (AVCN), posteroventral (PVCN), and dorsal (DCN) regions, as in other mammals. AVCN was characterized by bushy cells and stellate cells. The "bushy" dendritic trees of adjacent bushy cells often overlapped. PVCN was characterized by octopus, elongate, and stellate cells. The dendritic trees of adjacent octopus cells extended in a parallel array across the auditory nerve fibers. DCN had molecular, fusiform and polymorphic layers. The fusiform cell layer was especially prominent, with the fusiform cells appearing visually to be the organizing elements in DCN. The large cells in DCN were the fusiform and giant neurons; the medium cells were the stellate and elongate neurons; the small cells were the cartwheel, small stellate, and granule cells. The cochlear nucleus of rabbit is essentially similar in cytoarchitectural organization to other mammalian species which have been studied. The detailed morphology of the various cell types seen in Golgi preparations is quite similar to that of cat (Brawer et al., '74), although some differences do exist.

Animals↗

Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus.

The dorsal cochlear nucleus integrates acoustic with multimodal sensory inputs from widespread areas of the brain. Multimodal inputs are brought to spiny dendrites of fusiform and cartwheel cells in the molecular layer by parallel fibers through synapses that are subject to long-term potentiation and long-term depression. Acoustic cues are brought to smooth dendrites of fusiform cells in the deep layer by auditory nerve fibers through synapses that do not show plasticity. Plasticity requires Ca(2+)-induced Ca(2+) release; its sensitivity to antagonists of N-methyl-d-aspartate and metabotropic glutamate receptors differs in fusiform and cartwheel cells.

Animals↗

Immunolocalization of alpha4 and alpha7 subunits of nicotinic receptor in rat cochlear nucleus.

The rat cochlear nucleus (CN) is known to receive cholinergic input. To investigate the prevalence of nicotinic acetylcholine receptor (nAChR), immunohistochemistry for alpha4 and alpha7 subunits, which represent nAChRs with high binding affinities for nicotine and alpha-bungarotoxin, respectively, was performed on perfusion-fixed rat brain sections. Microscopic observations and densitometric measurements show dense labeling for alpha7 but not alpha4. Within the CN, alpha7 receptors are found in all subregions, with relatively high densities in granular regions. The distribution of alpha7 within the CN appears to correlate more closely with that of acetylcholinesterase than with mAChR or choline acetyltransferase. Our results suggest a role of nicotinic cholinergic transmission in the rat CN associated with high affinity for alpha-bungarotoxin.

Acetylcholinesterase↗

Differential distribution of synaptic endings containing glutamate, glycine, and GABA in the rat dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) integrates the synaptic information depending on the organization of the excitatory and inhibitory connections. This study provides, qualitatively and quantitatively, analyses of the organization and distribution of excitatory and inhibitory input on projection neurons (fusiform cells), and inhibitory interneurons (vertical and cartwheel cells) in the DCN, using a combination of high-resolution ultrastructural techniques together with postembedding immunogold labeling. The combination of ultrastructural morphometry together with immunogold labeling enables the identification and quantification of four major synaptic inputs according to their neurotransmitter content. Only one category of synaptic ending was immunoreactive for glutamate and three for glycine and/or gamma-aminobutyric-acid (GABA). Among those, nine subtypes of synaptic endings were identified. These differed in their ultrastructural characteristics and distribution in the nucleus and on three cell types analyzed. Four of the subtypes were immunoreactive for glutamate and contained round synaptic vesicles, whereas five were immunoreactive for glycine and/or GABA and contained flattened or pleomorphic synaptic vesicles. The analysis of the distribution of the nine synaptic endings on the cell types revealed that eight distributed on fusiform cells, six on vertical cells and five on cartwheel cells. In addition, postembedding immunogold labeling of the glycine receptor alpha1 subunit showed that it was present at postsynaptic membranes in apposition to synaptic endings containing flattened or pleomorphic synaptic vesicles and immunoreactive for glycine and/or GABA on the three cells analyzed. This information is valuable to our understanding of the response properties of DCN neurons.

Animals↗

Vertical cell responses to sound in cat dorsal cochlear nucleus.

The dorsal cochlear nucleus receives input from the auditory nerve and relays acoustic information to the inferior colliculus. Its principal cells receive two systems of inputs. One system through the molecular layer carries multimodal information that is processed through a neuronal circuit that resembles the cerebellum. A second system through the deep layer carries primary auditory nerve input, some of which is relayed through interneurons. The present study reveals the morphology of individual interneurons and their local axonal arbors and how these inhibitory interneurons respond to sound. Vertical cells lie beneath the fusiform cell layer. Their dendritic and axonal arbors are limited to an isofrequency lamina. They give rise to pericellular nests around the base of fusiform cells and their proximal basal dendrites. These cells exhibit an onset-graded response to short tones and have response features defined as type II. They have tuning curves that are closed contours (0 shaped), thresholds approximately 27 dB SPL, spontaneous firing rates of approximately 0 spikes/s, and they respond weakly or not at all to broadband noise, as described for type II units. Their responses are nonmonotonic functions of intensity with peak responses between 30 and 60 dB SPL. They also show a preference for the high-to-low direction of a frequency sweep. It has been suggested that these circuits may be involved in the processing of spectral cues for the localization of sound sources.

Acoustic Stimulation↗

Effects of contralateral sound stimulation on unit activity of ventral cochlear nucleus neurons.

The cochlear nucleus (CN) commissural connection represents the first opportunity for convergence of binaural information in the auditory brainstem. All major neuron types in the ventral CN (VCN) are innervated by a diverse population of cells in the contralateral VCN. This study examined the effect of contralateral sound stimulation on the spontaneous rates (SRs) of neurons in the VCN. Unit activity was recorded with silicon-substrate multichannel probes which allowed recordings from up to 16 sites simultaneously. On average, 30% of units showed short-latency (often only 2 ms greater than the latencies of ipsilateral sound-evoked responses) inhibition of SR by wideband contralateral noise bursts. Fewer units (4.5%) were excited by contralateral noise at sound levels low enough to exclude excitation by acoustic crossover. Both regular and irregular units in the anterior VCN (AVCN) and posterior VCN (PVCN) were inhibited by contralateral sound. Decrements in SR followed a monotonic function with increases in contralateral sound level, except where responses could be attributed to acoustic crossover. Restricting the contralateral noise bandwidth resulted in a frequency-specific inhibition, dominated by frequencies at and below the ipsilateral BF of the unit, consistent with anatomical findings of the tonotopic organization of the CN commissural pathway. The latencies of these effects are compatible with mono, di and tri-synaptic connections reflecting CN commissural pathway effects.

Acoustic Stimulation↗

Neural timing, inhibition and the nature of stellate cell interaction in the ventral cochlear nucleus.

The ventral cochlear nucleus (VCN) stellate cell population comprises two clusters: narrowly-tuned, excitatory T stellate neurons, and D stellate neurons, a broadly-tuned population of inhibitory cells. These neurons respond to best frequency (BF) tone bursts in a chopper or onset manner, respectively. Through extensive local and commissural projections the D stellate population provides a source of fast inhibitory input to both intrinsic and contralateral T stellate neurons. Whilst the nature of interactions between intrinsic stellate populations is difficult to examine, our previous intracellular investigations of the commissural pathway have provided a means by which to study this relationship in the in vivo preparation. It is the aim of this paper to both review and extend our understanding of the link between stellate populations and their involvement in the commissural pathway by presenting an overview of the results attained in our recently expanded study. The sample of 17 intracellular and 34 extracellular onset chopper (O(C)) and late/ideal (On(L)/On(I)) neurons revealed antidromic activity in 31.4% of neurons following contralateral stimulation, providing physiological evidence that On(L)/On(I) neurons also contribute projections to the commissural connection. Alternatively, 64.7% of the 34 intracellularly-recorded chopper neurons displayed fast, monosynaptic inhibitory potentials. This commissural input was found to influence the timing of neural activity in chopper neurons, providing insight into the relationship that exists between T and D stellate neurons.

Animals↗

Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) is a second-order auditory structure that also receives nonauditory information, including somatosensory inputs from the dorsal column and spinal trigeminal nuclei. Here we investigate the peripheral sources of the somatosensory inputs to DCN. Electrical stimulation was applied to cervical nerves C1-C8, branches of C2, branches of the trigeminal nerve, and hindlimb nerves. The largest evoked potentials in the DCN were produced by C2 stimulation and by stimulation of its branches that innervate the pinna. Electrical stimulation of C2 produced a pattern of inhibition and excitation of DCN principal cells comparable with that seen in previous studies with stimulation of the primary somatosensory nuclei, suggesting that the same pathway was activated. Because C2 contains both proprioceptive and cutaneous fibers, we applied peripheral somatosensory stimulation to identify the effective somatosensory modalities. Only stimuli that activate pinna muscle receptors, such as stretch or vibration of the muscles connected to the pinna, were effective in driving DCN units, whereas cutaneous stimuli such as light touch, brushing of hairs, and stretching of skin were ineffective. These results suggest that the largest somatosensory inputs to the DCN originate from muscle receptors associated with the pinna. They support the hypothesis that a role of the DCN in hearing is to coordinate pinna orientation to sounds or to support correction for the effects of pinna orientation on sound-localization cues.

Acoustic Stimulation↗

Differentiation of simple spike waveforms in the hamster dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) consists of many cell types with different morphologies and properties. DCN cells belonging to different morphological classes are distinguished by differences in their physiological characteristics such as their spectral and temporal response patterns, their levels of spontaneous activity, and certain biophysical properties. Recent studies suggest that they may also exhibit different action potentials, such as simple and complex spikes. In the present study, we systematically examined the spike waveforms of spontaneously active DCN neurons using extracellular recording methods. Neurons were found to exhibit simple spikes consisting of trains of individual action potentials. Spikes fell into two discrete groups of opposite polarity, those with M-shaped and those with W-shaped waveforms. The shapes of these waveforms recorded from a given unit remained constant, despite large changes in amplitude that occurred as the electrode was moved along its axis of penetration. A quantitative analysis of the fine details of the waveforms demonstrated that, although the durations of W- and M-shaped spikes exhibited considerable variation, the variants within each category fell along a continuous gradient rather than into discrete subgroups. Both M- and W-shaped waveforms were found predominantly in the fusiform cell and deep layers, with smaller numbers found in the dorsal acoustic stria. Consideration of their depths of occurrence, their response properties, and levels of spontaneous activity of the recorded neurons suggests that W-shaped waveforms probably are associated with fusiform cells, whereas M-shaped spikes likely originate from more than one cell type.

Action Potentials↗

Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) is a major brain center for integration of auditory information, and excitatory amino acid neurotransmission plays a central role in the processing of this information. In this study, the distribution of glutamate receptors was examined with preembedding immunocytochemistry, using 14 antibodies to ionotropic (GluR1, GluR2/3, GluR4, GluR5-7, GluR6/7, KA2, NR1, NR2A/B, delta 1/2) and metabotropic (mGluR1 alpha, mGluR2/3, mGluR5) glutamate receptor subtypes. Each of these antibodies produced a specific immunolabeling pattern, including a variety of postsynaptic, presynaptic, and glial localizations. Some antibodies showed widespread distribution patterns, notably the antibodies to the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptor subunits, GluR2 and GluR3, and the N-methyl-D-aspartate (NMDA) receptor subunit, NR1. In contrast, antibodies to other glutamate receptor subunits produced more restricted distribution patterns, especially that to GluR1, which stained the outer neuropil of the DCN, cartwheel cells, and a small population of presumptive interneurons associated with the dorsal acoustic stria, but produced little or no staining in fusiform cells or deep DCN neurons. Staining of the postsynaptic density and membrane of the granule cell-parallel fiber/cartwheel cell spins synapse was most prevalent with delta 1/2 and mGluR1 alpha antibodies. A unique pattern of staining was found with mGluR2/3 antibody--with staining concentrated in Golgi cells and unipolar brush cells of the middle to deep DCN. Distribution of some glutamate receptors in the DCN shows similarities to that of the cerebellum, where delta 2 and mGluR1 alpha may modulate neurotransmission at parallel fiber synapses, while mGluR2 and/or mGluR3 may modulate mossy terminal function.

Animals↗

Neuronal migration and differentiation in the development of the mouse dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) of mammals displays a cortical structure containing a number of cell types organized into distinct layers. In the present study, the migratory mode of large multipolar cells and granule cells as well as the morphological differentiation of the projection neurons were investigated in the development of the mouse DCN. The classification of the DCN neurons followed that of Ryugo and Willard. The mode of neuronal migration was examined by immunohistochemical bromodeoxyuridine labeling. Large multipolar neurons originated from the primary rhombic lip and small granule cells from the secondary rhombic lip. Large multipolar neurons migrated radially from the ventricular zone into the forming DCN. Granule cells were generated later than the large multipolar neurons and migrated via the subependymal and subpial routes. Large multipolar neurons and small granule cells were thus segregated early in the DCN development and intermixed later during perinatal maturation. Projection neurons retrogradely labeled by DiI application to the contralateral inferior colliculus showed neurite extension between the pial surface and the ventricular zone during migration in the DCN primordium. The retrogradely labeled projection neurons showed a well-differentiated morphology of the large multipolar neurons as early as the late embryonic stage. The arrangement of the radial glial processes coincided with that of the migratory projection neurons. The migratory immature neurons showed close apposition with the radial glial processes, suggesting that glial scaffolds are involved in the migration and settlement of the large multipolar neurons. Thus, it is suggested that the mode of migration and settlement of large multipolar neurons and granule cells in the developing DCN is highly similar to that of Purkinje and granule cell migration in the cerebellar development, based on the findings of this study and the structural similarity between the cerebellum and DCN.

Animals↗

Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) is rich in both glycine and GABA inhibitory neurotransmitter systems, and the response properties of its principal cells (pyramidal and giant cells) are strongly shaped by inhibitory inputs. For example, DCN principal cells often display highly nonmonotonic (so-called type IV) input-output functions in response to best-frequency (BF) tones. In this study, the inhibitory inputs onto the principal cell types and onto response types of known inhibitory interneurons were compared before and during iontophoretic application of the glycine- and GABA(A)-receptor antagonists, strychnine and bicuculline. Strychnine eliminates the central (on-BF) inhibitory area in type IV units, resulting in monotonic BF rate-level curves. Unexpectedly, bicuculline primarily enhances inhibition in principal-cell types; for example, type IV units are inhibited at lower sound levels in the presence of bicuculline. Principal cell types with weaker inhibitory inputs (type IV-T and type III units) are more strongly inhibited in the presence of bicuculline and usually are converted into type IV units. This enhancement of on-BF inhibition by bicuculline suggests a disinhibitory process involving GABA(A) action on a non-GABA(A)ergic inhibitory pathway. This latter pathway is probably glycinergic and involves type II units (deep-layer vertical cells) and/or complex-spiking units (superficial cartwheel cells) because both of these unit types are disinhibited by bicuculline. One intrinsic GABA(A) source could be the superficial stellate cells in DCN because bicuculline partly blocks the inhibition evoked by somatosensory-stimulated activation of the superficial granule-cell circuitry in DCN. Taken together, the results suggest that glycinergic circuits mediate directly the inhibition of DCN principal cells, but that GABA(A)ergic circuits modulate the strength of the inhibition.

Acoustic Stimulation↗

Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching.

We studied the chick auditory system to determine whether there is a normal developmental reduction in the number of cochlear nerve axons innervating individual cochlear nucleus (nucleus magnocellularis, NM) neurons. We also examined the preterminal branching patterns of cochlear nerve axons during development. The number of cochlear nerve axons innervating individual NM neurons was estimated by counting the increments in the postsynaptic response as the intensity of cochlear nerve electrical stimulation was varied gradually; this number fell from a mean of 4.0 on embryonic day 13 (E13) to a mean of 2.2 on E17 and E18 and the 4th day after hatching. This highly reliable decline in functional convergence was accompanied by a decrease in the number of preterminal branches of cochlear nerve fibers innervating the NM. On E13 and E14, most axons stained by iontophoretic injections of horseradish peroxidase showed two distinct preterminal branches in the NM. By E17 and E18 and thereafter, cochlear nerve axons were unbranched and terminated with a characteristic single large calycine ending in the NM. There are about twice as many cochlear nerve axons as neurons in the NM and the number of fibers in the nerve appears to decline only slightly between E13 and E17. The 50% decline in the number of cochlear nerve axons making functional synapses on individual NM neurons therefore is associated principally with the concurrent elimination of cochlear nerve axon branching in the NM.

Animals↗

Differential expression of N-methyl-D-aspartate receptor in the cochlear nucleus of the mouse.

Glutamate is used in the cochlear nucleus as a neurotransmitter by cochlear nerve synapses and by local circuits of granule cell axons. In the present study, immunocytochemistry and in situ hybridization were used to identify different types of neurons expressing N-methyl-D-aspartate receptor subunit I (NMDAR1) in the mouse cochlear nucleus. N-Methyl-D-aspartate receptor subunit 1 was expressed in most neuronal types, but granule cells in the dorsal cochlear nucleus had little, if any, expression, unlike their heavily labeled counterparts in the small cell shell and cerebellum. The findings do not support an analogy between the dorsal cochlear nucleus and the cerebellar cortex. In the cochlear nucleus the most heavily labeled structures were dendrites in the small cell shell and superficial dorsal cochlear nucleus, including the fusiform cell apical dendrites, which are targets of granule cell axons. However, fusiform cell basal dendrites, which are the synaptic sites of cochlear nerve fibers, did not express N-methyl-D-aspartate receptor subunit 1. Thus different parts of the fusiform cells can have different subunits in their glutamate receptors. Also branches of the same cochlear nerve axons projecting to the octopus, stellate, and bushy cells of the ventral cochlear nucleus can use N-methyl-D-aspartate receptor, while their branches to fusiform cells cannot. Each cochlear nucleus neuron type has a characteristic level of N-methyl-D-aspartate receptor subunit 1 expression. Each type differs in its auditory response properties, which may depend on synaptic activities requiring different glutamate subunit patterns.

Animals↗

Transient focal cooling at the round window and cochlear nucleus shows round window CAP originates from cochlear neurones alone.

We have measured the compound action potential (CAP) evoked by very brief high-frequency tone-bursts (20 kHz, 1/4 ms) at the round window (RW) and at the surface of the cochlear nucleus (CN) in guinea pigs before, during and after a localised chilling of either the cochlea or CN, with a non-toxic 'freeze spray'. CN chilling almost abolished the negative-going component of the CAP measured in the CN (generated by the CN and here called the cochlear nucleus response or CNR), leaving a positive-going localised response from the cochlear neurones as they leave the internal auditory meatus. Within 3 min, the CNR recovered to control values. During that time, the N(1) component of the RW CAP was slightly increased and the P(1) was larger, even though the CNR was abolished, indicating that the P(1) was not due to electrotonic spread of current from the CN. The N(2) and successive peaks at the RW were also abolished, but returned after 30 s. When the cochlea was chilled, the RW CAP was initially reduced in amplitude, presumably due to a drop in the number of cochlear neurones spiking in response to sound, but recovered within 3 min to be larger than the control waveform, with a more prominent N(1) peak which was delayed slightly, making the CAP more monophasic. At the same time, the CNR was smaller, presumably due to fewer cochlear neurones responding, but overall the CN CAP was altered little in waveshape. These experiments indicate that that RW CAP is generated almost solely by cochlear neurones. We also suggest that some of the changes in the RW CAP during the chills were due to changes in the firing of the lateral olivo-cochlear system of efferent neurons.

Acoustic Stimulation↗

Projections of the pontine nuclei to the cochlear nucleus in rats.

In the cochlear nucleus, there is a magnocellular core of neurons whose axons form the ascending auditory pathways. Surrounding this core is a thin shell of microneurons called the granule cell domain (GCD). The GCD receives auditory and nonauditory inputs and projects in turn to the dorsal cochlear nucleus, thus appearing to serve as a central locus for integrating polysensory information and descending feedback. Nevertheless, the source of many of these inputs and the nature of the synaptic connections are relatively unknown. We used the retrograde tracer Fast Blue to demonstrate that a major projection arises from the contralateral pontine nuclei (PN) to the GCD. The projecting cells are more densely located in the ventral and rostral parts of the PN. They also are clustered into a lateral and a medial group. Injections of anterograde tracers into the PN labeled mossy fibers in the contralateral GCD. The terminals are confined to those parts of the GCD immediately surrounding the ventral cochlear nucleus. There is no PN projection to the dorsal cochlear nucleus. These endings have the form of bouton and mossy fiber endings as revealed by light and electron microscopy. The PN represent a key station between the cerebral and cerebellar cortices, so the pontocochlear nucleus projection emerges as a significant source of highly processed information that is introduced into the early stages of the auditory pathway. The cerebropontocerebellar pathway may impart coordination and timing cues to the motor system. In an analogous way, perhaps the cerebropontocochlear nucleus projection endows the auditory system with a timing mechanism for extracting temporal information.

Animals↗