The inferior colliculus (IC) processes auditory information ascending from the brainstem. The response of the IC to this information and its ability to transform it is partly determined by the types of ionic currents that generate the intrinsic discharge patterns of IC neurons and their susceptibility to changes in the external environment. We have used whole-cell patch-clamp techniques on IC neurons in rat brain slices to characterize the potassium currents present and to correlate them with the firing patterns observed. Neurons in the IC can be classified into six physiologically distinct cell types. Each of these cell types has a firing pattern that is generated by a unique potassium current and set of cellular parameters. The inferior colliculus (IC) receives information about sound from the lower brainstem and sends it to the auditory cortex via the medial geniculate body. Neurons in the IC are faced with integrating information from numerous inhibitory synapses, often with latencies that are shorter than the excitatory synapses (Kuwada et al., 1997). The ability of the IC to integrate these inputs will be determined, in part, by the physiological state of each IC neuron at the time it receives synaptic input. This physiological state, and the resultant extent to which the IC modifies the synaptic information it receives, will be shaped by its discharge pattern and the modifiability of the ionic currents that underlie its firing. The ability of IC neurons to integrate synaptic information will depend on the nature of the voltage-and calcium (Ca 2ϩ )-gated potassium (K ϩ ) channels that underlie its discharge pattern. For example, Ca 2ϩ -dependent K ϩ currents have been hypothesized to contribute to the adaptation exhibited by some IC neurons (Cai et al., 1998). This adaptation may be the means by which the IC codes interaural phase modulation (McAlpine et al., 2000). Adaptation is an intrinsic feature of some IC neurons (Wagner, 1994;Peruzzi et al. 2000), but the underlying ionic mechanisms have not been explored. Other IC neurons exhibit a pause in the onset of sustained firing (pause-build firing pattern) (Kuwada et al., 1984(Kuwada et al., , 1997Rees et al., 1997;Peruzzi et al. 2000), which may be evoked by either synaptic inhibition or the intrinsic afterhyperpolarization of the cell. An A-type K current has been shown to underlie similar pause-build firing patterns in other systems (Connor and Stevens, 1971a,b;Neher, 1971;Kim et al., 1994;Kanold and Manis, 1999), but the presence of A-currents has not been shown in the IC. Onset and regularly firing sustained neurons are also intrinsically exhibited firing patterns in the IC (Peruzzi et al., 2000), and these cells may use other types of ionic conductances, not yet identified, to integrate synaptic information.In this study, we have used the whole-cell patch-clamp technique (Hamill et al., 1981) to examine the ionic currents that trigger the firing patterns of IC neurons. Based on the firing patterns in response to depolarizing and hyperpolarizing curre...
The goal was to investigate possible monosynaptic GABAergic projections from the inferior colliculus (IC) to thalamocortical neurons of the medial geniculate body (MGB) in the rat. Although there is little evidence for such a projection in other sensory thalamic nuclei, a GABAergic, ascending auditory projection was reported recently in the cat. In the present study, immunohistochemical and tract-tracing methods were used to identify neurons in the IC that contain GABA and project to the MGB. GABA-positive projection neurons were most numerous in the central nucleus and less so in the dorsal and lateral cortex. They were rare in the lateral tegmental system and brachium of the IC. The dorsal nucleus of the lateral lemniscus also contained GABA-positive projection neurons. In brain slices, stimulation of the brachium produced monosynaptic inhibitory postsynaptic potentials in morphologically identified thalamocortical relay neurons. The inhibitory potentials cannot originate locally, because they persisted when ionotropic glutamatergic transmission was blocked. Typically, brachium stimulation elicited a GABA A -mediated inhibitory potential followed by an excitatory potential and a longer latency GABA Bmediated inhibitory potential.We conclude that the GABA-containing neurons of the IC make short-latency, monosynaptic inputs to the thalamocortical projection neurons in the MGB. Such inputs may distinguish the main auditory pathway from indirect or tegmental auditory pathways as well as from other sensory systems. Monosynaptic inhibitory inputs to the medial geniculate may be important for the regulation of firing patterns in thalamocortical neurons. Key words: auditory pathway; retrograde tracing; brain slice preparation; immunohistochemistry; thalamus; midbrain; reticular formation; dorsal nucleus of the lateral lemniscusRecently, a novel and strong GABA-positive input from the inferior colliculus (IC) has been demonstrated in the cat medial geniculate body (MGB) . Thus, thalamocortical neurons in the MGB may receive monosynaptic, GABA-mediated inputs from the brainstem, in contrast to the neurons of other sensory thalamic nuclei. In most thalamic nuclei, inhibitory inputs come from local interneurons or intrathalamic neurons (for review, see Sherman and Koch, 1986;Steriade and Llinas, 1988). For example, in the lateral geniculate body, ascending inputs can excite directly the interneurons, which in turn inhibit thalamocortical neurons (Hirsch and Burnod, 1987;Lindstrom and Wrobel, 1990;Soltesz and Crunelli, 1992;Pape and McCormick, 1995). Such a scenario is less likely in the rat MGB. There are few local GABAergic interneurons, yet many GABA-positive axonal boutons are present Larue, 1988, 1996). This suggests that inhibitory influences arise outside the MGB. Our goal in this study was to identify and characterize one such inhibitory input in the rat.To test whether thalamocortical neurons of the MGB receive monosynaptic GABAergic input from the lower brainstem, we used both anatomical and electrophysiological...
The laminar organization of the central nucleus of inferior colliculus includes layers of axons that may be important in shaping the responses of neurons. Depending on their source, some layered axons are afferents that are superimposed and terminate on the same postsynaptic neurons, while other layered afferents, such as those from the ipsilateral and contralateral lateral superior olive, terminate side-by-side. The specific pattern of convergence may dictate which populations of axons are presynaptic to layered disc-shaped neurons in the central nucleus. We compared the distribution of afferent axons from the dorsal cochlear nucleus and the lateral superior olive to the contralateral inferior colliculus in the cat. Injection sites in cochlear nucleus and superior olive were physiologically characterized by extracellular recordings of single and multiple units in response to monaural and binaural acoustic stimulation. Two separate injections were made in each case, and both injection sites contained units with overlapping best frequencies. Biotinylated dextran, fluorescent dextran, 3H-leucine, and wheat germ agglutinin conjugated to horseradish peroxidase were used as anterograde tracers. The present results show that layered axons from the dorsal cochlear nucleus and lateral superior olive are superimposed in part of the contralateral central nucleus. Both projections were arranged in rostro-caudally oriented axonal layers that converged in the ventral part of the central nucleus. However, in the dorsal part of the central nucleus, the same layer of axons from the dorsal cochlear nucleus did not terminate with afferents from the lateral superior olive. Within the overlapping layers in the ventral central nucleus, the overlap of axons from the dorsal cochlear nucleus and the lateral superior olive was uniform except for small patches that were usually smaller than the dendritic fields of disc-shaped neurons. These data suggest that the layers may create specific functional zones in the central nucleus of the inferior colliculus. One zone may contain neurons with binaural responses that combine the properties of the inputs from the contralateral lateral superior olive and the dorsal cochlear nucleus. A second zone may contain inputs from the cochlear nucleus but lack those of the lateral superior olive.
The inferior colliculus (IC) is a major auditory structure that integrates synaptic inputs from ascending, descending, and intrinsic sources. Intracellular recording in situ allows direct examination of synaptic inputs to the IC in response to acoustic stimulation. Using this technique and monaural or binaural stimulation, responses in the IC that reflect input from a lower center can be distinguished from responses that reflect synaptic integration within the IC. Our results indicate that many IC neurons receive synaptic inputs from multiple sources. Few, if any, IC neurons acted as simple relay cells. Responses often displayed complex interactions between excitatory and inhibitory sources, such that different synaptic mechanisms could underlie similar response patterns. Thus, it may be an oversimplification to classify the responses of IC neurons as simply excitatory or inhibitory, as is done in many studies. In addition, inhibition and intrinsic membrane properties appeared to play key roles in creating de novo temporal response patterns in the IC.
It is known that the dorsal cochlear nucleus and medial geniculate body in the auditory system receive significant inputs from somatosensory and visual-motor sources, but the purpose of such inputs is not totally understood. Moreover, a direct connection of these structures has not been demonstrated, because it is generally accepted that the inferior colliculus is an obligatory relay for all ascending input. In the present study, we have used auditory neurophysiology, double labeling with anterograde tracers, and retrograde tracers to investigate the ascending projections of the cochlear nuclear complex. We demonstrate that the dorsal cochlear nucleus and the small cell cap of the ventral cochlear nucleus have a direct projection to the medial division of the medial geniculate body. These direct projections from the cochlear nucleus complex bypass the inferior colliculus and are widely distributed within the medial division of the medial geniculate, suggesting that the projection is not topographic. As a nonlemniscal auditory pathway that parallels the conventional auditory lemniscal pathway, its functions may be distinct from the perception of sound. Because this pathway links the parts of the auditory system with prominent nonauditory, multimodal inputs, it may form a neural network through which nonauditory sensory and visual-motor systems may modulate auditory information processing.
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