Two classes of GABAergic neurons in the inferior colliculus.

The inferior colliculus (IC) is unique, having both glutamatergic and GABAergic projections ascending to the thalamus. Although subpopulations of GABAergic neurons in the IC have been proposed, criteria to distinguish them have been elusive and specific types have not been associated with specific neural circuits. Recently, the largest IC neurons were found to be recipients of somatic terminals containing vesicular glutamate transporter 2 (VGLUT2). Here, we show with electron microscopy that VGLUT2-positive (VGLUT2(+)) axonal terminals make axosomatic synapses on IC neurons. These terminals contain only VGLUT2 even though others in the IC have VGLUT1 or both VGLUT1 and 2. We demonstrate that there are two types of GABAergic neurons: larger neurons with VGLUT2(+) axosomatic endings and smaller neurons without such endings. Both types are present in all subdivisions of the IC, but larger GABAergic neurons with VGLUT2(+) axosomatic terminals are most prevalent in the central nucleus. The GABAergic tectothalamic neurons consist almost entirely of the larger cells surrounded by VGLUT2(+) axosomatic endings. Thus, two types of GABAergic neurons in the IC are defined by different synaptic organization and neuronal connections. Larger tectothalamic GABAergic neurons are covered with glutamatergic axosomatic synapses that could allow them to fire rapidly and overcome a slow membrane time constant; their axons may be the largest in the brachium of the IC. Thus, large GABAergic neurons could deliver IPSPs to the medial geniculate body before EPSPs from glutamatergic IC neurons firing simultaneously.

Learning drives differential clustering of axodendritic contacts in the barn owl auditory system.

Computational models predict that experience-driven clustering of coactive synapses is a mechanism for information storage. This prediction has remained untested, because it is difficult to approach through time-lapse analysis. Here, we exploit a unique feature of the barn owl auditory localization pathway that permits retrospective analysis of prelearned and postlearned circuitry: owls reared wearing prismatic spectacles develop an adaptive microcircuit that coexists with the native one but can be analyzed independently based on topographic location. To visualize the clustering of axodendritic contacts (potential synapses) within these zones, coactive axons were labeled by focal injection of fluorescent tracer and their target dendrites labeled with an antibody directed against CaMKII (calcium/calmodulin-dependent protein kinase type II, alpha subunit). Using high-resolution confocal imaging, we measured the distance from each contact to its nearest neighbor on the same branch of dendrite. We found that the distribution of intercontact distances for the adaptive zone was shifted dramatically toward smaller values compared with distributions for either the maladaptive zone of the same animals or the adaptive zone of normal juveniles, which indicates that a dynamic clustering of contacts had occurred. Moreover, clustering in the normal zone was greater in normal juveniles than in prism-adapted owls, indicative of declustering. These data demonstrate that clustering is bidirectionally adjustable and tuned by behaviorally relevant experience. The microanatomical configurations in all zones of both experimental groups matched the functional circuit strengths that were assessed by in vivo electrophysiological mapping. Thus, the observed changes in clustering are appropriately positioned to contribute to the adaptive strengthening and weakening of auditory-driven responses.

Descending projections from the inferior colliculus to medial olivocochlear efferents: Mice with normal hearing, early onset hearing loss, and congenital deafness.

Auditory efferent neurons reside in the brain and innervate the sensory hair cells of the cochlea to modulate incoming acoustic signals. Two groups of efferents have been described in mouse and this report will focus on the medial olivocochlear (MOC) system. Electrophysiological data suggest the MOC efferents function in selective listening by differentially attenuating auditory nerve fiber activity in quiet and noisy conditions. Because speech understanding in noise is impaired in age-related hearing loss, we asked whether pathologic changes in input to MOC neurons from higher centers could be involved. The present study investigated the anatomical nature of descending projections from the inferior colliculus (IC) to MOCs in 3-month old mice with normal hearing, and in 6-month old mice with normal hearing (CBA/CaH), early onset progressive hearing loss (DBA/2), and congenital deafness (homozygous Shaker-2). Anterograde tracers were injected into the IC and retrograde tracers into the cochlea. Electron microscopic analysis of double-labelled tissue confirmed direct synaptic contact from the IC onto MOCs in all cohorts. These labelled terminals are indicative of excitatory neurotransmission because they contain round synaptic vesicles, exhibit asymmetric membrane specializations, and are co-labelled with antibodies against VGlut2, a glutamate transporter. 3D reconstructions of the terminal fields indicate that in normal hearing mice, descending projections from the IC are arranged tonotopically with low frequencies projecting laterally and progressively higher frequencies projecting more medially. Along the mediolateral axis, the projections of DBA/2 mice with acquired high frequency hearing loss were shifted medially towards expected higher frequency projecting regions. Shaker-2 mice with congenital deafness had a much broader spatial projection, revealing abnormalities in the topography of connections. These data suggest that loss in precision of IC directed MOC activation could contribute to impaired signal detection in noise.

Synaptogenesis in the inferior colliculus of the pre-hearing postnatal ferret.

Although intrinsic organization in the inferior colliculus (IC) has been surveyed in a variety of species, current knowledge of synaptogenesis within the mammalian inferior colliculus is limited. The present study surveyed the ultrastructure of the central nucleus of the inferior colliculus in postnatal day (P) P4, P7, P14, and P28 ferrets, prior to the onset of hearing at the end of the first postnatal month with the goal of beginning to characterize the time course of synapse formation in relation to the development of afferent projection patterns within the IC. Results suggest that initial synaptogenesis has occurred in the IC by P4 and continues during the period when maturation of the distribution of axons from brainstem auditory nuclei is taking place.

Tectothalamic inhibitory projection neurons in the avian torus semicircularis.

Inhibitory feedforward projection is one of key features of the organization of the central auditory system. In mammals, the inferior colliculus (IC) is the origin of a substantial inhibitory feedforward projection as well as an excitatory projection to the auditory thalamus. This inhibitory feedforward projection is provided by large γ-aminobutyric acid (GABA)ergic (LG) neurons, which are characterized by their receipt of dense excitatory axosomatic terminals positive for vesicular glutamate transporter (VGLUT) 2. In the avian torus semicircularis (TS), which is the homolog of the IC, neither the homology of cell types nor the presence of inhibitory feedforward inhibition have been established. In this study, we tested the presence of LG neurons in pigeon and chicken by neuroanatomical techniques. The TS contained two types of GABAergic neurons of different soma size. Of these, larger GABA + cells were encircled by dense VGLUT2 + axosomatic terminals. Ultrastructural analyses revealed that more than 30% of the perimeter of a large GABA+, but not small GABA + or GABA-, soma was covered by presumptive excitatory axosomatic terminals, suggesting that large GABA + cells are the sole recipient of dense excitatory axosomatic synapses. After injection of a retrograde tracer into the auditory thalamus, many retrogradely labeled neurons were found bilaterally in the TS, a few of which were GABA+. Almost all tectothalamic GABA + neurons had large somata, and received dense VGLUT2 + axosomatic terminals. These results clearly demonstrated the presence of LG neurons in birds. The similar morphology of LG neurons implies that the function of tectothalamic inhibition is similar among amniotes. J. Comp. Neurol. 524:2604-2622, 2016. © 2016 Wiley Periodicals, Inc.

Effects of long-term salicylate administration on synaptic ultrastructure and metabolic activity in the rat CNS.

Tinnitus is associated with neural hyperactivity in the central nervous system (CNS). Salicylate is a well-known ototoxic drug, and we induced tinnitus in rats using a model of long-term salicylate administration. The gap pre-pulse inhibition of acoustic startle test was used to infer tinnitus perception, and only rats in the chronic salicylate-treatment (14 days) group showed evidence of experiencing tinnitus. After small animal positron emission tomography scans were performed, we found that the metabolic activity of the inferior colliculus (IC), the auditory cortex (AC), and the hippocampus (HP) were significantly higher in the chronic treatment group compared with saline group (treated for 14 days), which was further supported by ultrastructural changes at the synapses. The alterations all returned to baseline 14 days after the cessation of salicylate-treatment (wash-out group), indicating that these changes were reversible. These findings indicate that long-term salicylate administration induces tinnitus, enhanced neural activity and synaptic ultrastructural changes in the IC, AC, and HP of rats due to neuroplasticity. Thus, an increased metabolic rate and synaptic transmission in specific areas of the CNS may contribute to the development of tinnitus.

Morphology of the inferior colliculus in C57BL/6J and CBA/J mice across the life span.

Basic anatomical features were evaluated in the inferior colliculus (IC) of C57BL/6J and CBA/J mice across the adult life span (1.5 to 30 months of age). C57BL/6J mice exhibit progressive age-related cochlear pathology and become severely hearing-impaired during the second year of life; CBA/J mice exhibit little hearing loss as they age. Age had little effect on the size of the IC, the size of IC neurons, or the packing density of IC neurons and there was no evidence of age-related neuron loss. However, old CBA/J mice developed numerous spongiform lesions throughout the brainstem. The absence of morphological changes in the IC of hearing-impaired C57BL/6J mice supports the hypothesis that features such as the size of neurons, survival of neurons, and volume of the neuropil are not affected by chronic sensorineural pathology in central auditory nuclei (e.g., as the IC) that do not receive direct input from primary afferent fibers. The data from both strains taken together indicate that certain basic anatomical properties of the mouse IC persist in the face of aging.

Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig.

We present a comprehensive description of the local (intrinsic and commissural) connections in the central nucleus of the inferior colliculi (CNICs) in guinea pig. Focal injections of the anterograde tracer biocytin were made into physiologically identified loci of the CNIC and the spatial organisation of the labeled fibres was revealed with computer-assisted three-dimensional (3-D) reconstruction. The intrinsic fibres form a series of V-shaped laminar plexuses composed of fibres bearing both terminal and en passant boutons. Each laminar plexus has a central wing located in the CNIC that extends into the dorsal cortex and an external wing located in the external cortex. The edge where the two wings intersect delimits the lateral border of the central nucleus with the external cortex. The density of labeled terminals was consistently lower in the cortices than in the CNIC. The laminar plexus connects points of similar frequency within the CNIC. Seen in 3-D, the location, orientation, shape, and area of the laminar plexus vary as a function of best frequency. The commissural fibres ending in the contralateral IC to the injection also form a laminar plexus which is symmetrical to the ipsilateral plexus. Electrolytic lesions placed in the contralateral IC at sites with best frequencies corresponding to those of the injection coincided with the terminals of the commissural fibres in most instances. Possible patterns for the organisation of these connections (point-to-point and diverging) are discussed. Three systems of peripheral axons to the laminar plexus are described: parallel, oblique, and perpendicular to the central wing. The novel parallel system has terminals in both ICs that run parallel to the central wing. It might constitute the anatomical basis for across-frequency interactions. The oblique and perpendicular systems are fibres of passage projecting to the commissure and brachium of the IC, respectively.

Morphology of retinal axon arbors induced to arborize in a novel target, the medial geniculate nucleus. II. Comparison with axons from the inferior colliculus.

Specific neonatal lesions in ferrets can induce retinal axons to project into the medial geniculate nucleus (MGN). In the accompanying paper (Pallas et al., this issue), we described the morphology of these retinal ganglion cell axons. Those results and others (Roe et al. [1993] J. Comp. Neurol. 334:263) suggest that these axons belong to the W class of retinal axons. In this paper, the retino-MGN axons are compared with the normal inputs to the MGN from the brachium of the inferior colliculus (BIC). We first sought to determine further the extent to which a novel target might influence retinal axon arbor morphology. The second issue concerns retinal topography. Ferrets with retinal projections to the MGN have a two-dimensional retinotopic map in the MGN and the primary auditory cortex rather than the one-dimensional tonotopic map normally present (Roe et al. [1990] Science 250:818). To investigate whether there might be an anatomical substrate for a two-dimensional retinotopic map in the MGN, we compared the space-filling characteristics of the retino-MGN axons with the IC-MGN axons. Our results show that the branched retino-MGN axons resemble normal retinal W axons much more closely than they resemble the normal inputs to MGN. In addition, most of the axon arbors from the BIC are elongated along the rostrocaudal (isofrequency) axis, whereas the branched retino-MGN axons are more spatially restricted, suggesting an anatomical substrate for a retinotopic map in the MGN of the rewired ferrets.

Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat.

The dendritic and axonal morphology of neurons in the inferior colliculus of the cat was investigated after intracellular injection of HRP, in vivo. All injected axons gave off local collaterals, and most showed a widespread distribution and lacked a specific orientation. In contrast, the dendrites of injected neurons were distinguished by their degree of orientation and the direction of the longest axis of orientation. Dendrites showed a high, moderate, or low degree of orientation. Most highly oriented cells had their longest axis in the rostrocaudal direction with fewer in the mediolateral direction. In the central nucleus, only the rostrocaudally oriented cells correspond to the disc-shaped cells identified in Golgi preparations. Unlike most cells in our sample, the two cells that were disc-shaped had axons that were parallel to the orientation of the dendritic tree. In the dorsal cortex, rostrocaudally oriented cells also were found, but they had unoriented axons. In both the central nucleus and dorsal cortex, cells with a mediolateral axis of orientation or no specific orientation correspond to stellate cells and had axons with widespread local collaterals. These results suggest that an extensive network of local axon collaterals may contribute to neural processing within the inferior colliculus. In the central nucleus, local axons may establish connections within or across the fibrodendritic laminae. In the dorsal cortex, the local and afferent axons may form a complex reticular network. Finally, some injected cells had axons terminating locally and also entering the brachium of the inferior colliculus. This suggests that cells in the inferior colliculus may function as both interneurons and projection neurons.

The morphological development of the inferior colliculus in a marsupial, the Northern quoll (Dasyurus hallucatus).

As a part of a project concerning the development of hearing, some features of the morphological development of the inferior colliculus were studied in a marsupial, the Northern quoll or native cat (Dasyurus hallucatus). Marsupials are of particular interest in developmental studies because much embryonic development occurs outside the uterus, in the pouch. Nissl-stained material was prepared from pouch-young at various ages between 11 and 81 days, and for a number of adults. Four pouch-young were injected with tritiated thymidine and killed later during pouch life. The inferior colliculus is first recognizable in pouch-young aged 23 days, when it is bordered by a cell-sparse ring of tissue. By this time, the labelling patterns following injections of tritiated thymidine made on days 7-9 suggest that migration of cells to the inferior colliculus from the ventricular germinal zone has been largely completed. At 81 days, close to the time when the young move out of the pouch, the adult cytoarchitecture--a central nucleus flanked by dorsal and lateral cortical regions--is clear. Cell areas expand monotonically as a function of age. The period of days 45-50 is associated with a large expansion of cell volume and a concomitant decrease in packing density. It is likely that functional connections are forming during this period, which may herald the onset of hearing in the quoll. Total cell numbers increase to a peak at day 36, fall to a minimum at day 50, and rise again to the adult value. The second increase is likely to be a phase of glial proliferation, in part associated with the onset of myelination. This increase correlates with departure of the young from the pouch.

Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography.

The superior olivary complex is the first site in the central auditory system where binaural interactions occur. The output of these nuclei is direct to the central nucleus of the inferior colliculus, where binaural inputs synapse with monaural afferents such as those from the cochlear nuclei. Despite the importance of the olivary pathways for binaural information processing, little is known about their synaptic organization in the colliculus. The present study investigates the structure of the projections from the lateral and medial superior olivary nuclei to the inferior colliculus at the electron microscopic level. Stereotaxic placement and electrophysiological responses to binaural sounds were used to locate the superior olive. Anterograde axonal transport of 3H-leucine was combined with light and electron microscopic autoradiography to reveal the location and morphology of the olivary axonal endings. The results show that the superior olivary complex contributes different patterns of synaptic input to the central nucleus of the inferior colliculus. Each projection from the superior olivary complex to the colliculus differs in the number and combinations of endings. Axonal endings from the ipsilateral medial superior olive were exclusively the round (R) type that contain round synaptic vesicles and make asymmetrical synaptic junctions. This morphology is usually associated with excitatory synapses and neurotransmitters such as glutamate. Endings from medial superior olive terminate densely in the central nucleus. The projection from the contralateral lateral superior olive also terminates primarily as R endings. This projection also includes small numbers of pleomorphic (PL) endings that contain pleomorphic synaptic vesicles and usually make symmetrical synaptic junctions. The PL morphology is associated with inhibitory synapses and transmitters such as gamma-aminobutyric acid and glycine. All endings from the contralateral lateral superior olive terminate much less densely than endings from the medial olive. In contrast, the projection from the ipsilateral lateral superior olive contributes both R and PL endings in roughly equal proportions. These ipsilateral afferents are heterogeneous in density and can terminate in lower or higher concentrations than endings from the contralateral side. These data show that the superior olive is a major contributor to the synaptic organization of the central nucleus of the inferior colliculus. The ipsilateral projections of the medial and lateral superior olive may produce higher concentrations of R endings than other inputs to the central nucleus. Such endings may participate in excitatory synapses. The highest concentrations of PL endings come from the ipsilateral lateral superior olive.(ABSTRACT TRUNCATED AT 400 WORDS)

Axonal morphology in fibrodendritic laminae of the dorsal nucleus of the lateral lemniscus: afferent projections from the medial superior olivary nucleus.

The distribution and morphology of axons projecting from the medial superior olivary nucleus to the dorsal nucleus of the lateral lemniscus were studied in the adult cat. Injections of Phaseolus vulgaris-leucoagglutinin, biocytin, or dextran-rhodamine in the medial superior olivary nucleus labeled axons that ascended in the lateral lemniscus. Before entering the inferior colliculus, collateral branches of these labeled axons ended in the dorsal nucleus of the lateral lemniscus in thin, horizontal bands forming laminae that extended throughout the rostral-caudal length of the dorsal nucleus of the lateral lemniscus. A dorsal-ventral topography was apparent in the position of the lamina with respect to the injection site, but no relation between the rostral-caudal location of labeled endings and the injection site was observed. There was a divergent pattern of connections within the horizontal laminae rather than a point-to-point organization. The terminal branches of the collateral axons exhibited round or oval boutons en passant and terminaux. Individual arbors reconstructed from serial sections distributed varicosities in circumscribed domains that were only a subcomponent of the area of the afferent laminae in which they were distributed. The spatial relationships of axonal domains of several axons labeled from a single injection in the medial superior olivary nucleus suggest a mosaic pattern in the laminar connections with the dorsal nucleus of the lateral lemniscus.

The central nucleus of the inferior colliculus in the cat.

The central nucleus of the inferior colliculus in the cat is distinguished by its unique neuropil. In Golgi-impregnated material, it is composed primarily of neurons with disc-shaped dendritic fields arranged into parallel arrays, or laminae, complemented by the laminar afferent axons from the lateral lemniscus. Large, medium-large, medium, and small varieties of disc-shaped cells are distinguished on the basis of the size of the dendritic field and cell body size, dendritic diameter, and dendritic appendages. A second major class of neurons in the central nucleus are the stellate cells with dichotomously branched, spherical-shaped dendritic trees. Simple, complex, and small stellate cells can be distinguished by their size and by the complexity of the dendritic and axonal branching. Laminar afferent axons are recognized by the nests of collateral side branches and the grapelike clusters of terminal boutons--thick, thin, and intermediate-sized varieties are apparent. Other axon types include local collaterals of central nucleus neurons, some of which are distinguished by their frequent and complex collaterals. In the central nucleus, the configuration of the fibrodendritic laminae, the presence of subdivisions, and the banding of afferent axons suggest levels of organization which are superimposed on the synaptic arrangements of the individual cell and axon types. The laminar pattern, as studied in serial Golgi-impregnated sections, differs from previous reports. The central nucleus contains subdivisions which can be distinguished by their laminar pattern, different proportions of cell types, and the packing density of the cell bodies and axonal plexus. The patterns of degeneration observed in Nauta-stained material after lesions of caudal auditory pathways show that thick and fine afferent fibers form dense bands of degeneration separated by sparse, fine-fiber degeneration. The bands are thicker than individual laminae but smaller than the subdivisions. The intrinsic organization of the neurons and axons, combined with the laminar organization, subdivisions, and banding patterns, each may contribute different aspects to the processing of auditory information in the central nucleus.

Quantitative analyses of axonal endings in the central nucleus of the inferior colliculus and distribution of 3H-labeling after injections in the dorsal cochlear nucleus.

Quantitative analyses of electron microscopic (EM) autoradiographs were used to identify the afferents from the dorsal cochlear nucleus in the central nucleus of the inferior colliculus (IC) in the cat. In order to localize the sources of radioactivity, material from axonal transport experiments was analyzed by means of a hypothetical grain procedure which takes the cross-scatter of beta particles into account. Measurements of the synaptic vesicles in axonal endings and a cluster analysis were used to identify different groups of endings. In order to determine which types of endings arise in the dorsal cochlear nucleus, axonal endings labeled after axonal transport and unlabeled endings were characterized and compared to the groups defined by the cluster analysis. Axonal endings with round synaptic vesicles were labeled with more than 2 grains/micron2 which was about 30% of the radioactivity in the central nucleus of the IC. This was six to seven times greater than if the radioactivity had been randomly distributed. Other tissue compartments usually had less radioactivity. Some myelinated and unmyelinated axons were labeled, but, as a group they had lower amounts of radioactivity than predicted by random labeling. In most cases, only low levels of activity were found in glial and postsynaptic structures. Five groups of axonal endings in the medial part of the central nucleus were identified by an analysis which clustered similar types of endings. The variance of the longest axis, the mean diameter, the variance of area, and the mean area of the synaptic vesicles were the variables most useful in distinguishing these five groups. Axonal endings with round synaptic vesicles were classified as either small, or large, or very large, while endings with pleomorphic vesicles were either large or small. Using measurements of the cross-sectional diameter of dendritic microtubules, samples of digitized axonal endings from normal and experimental cases were normalized and could be compared directly to the groups defined by the cluster analysis. Microtubules were 21.7 nm (+/- 1.6) in average diameter. After injections of 3H-leucine and/or proline in the dorsal cochlear nucleus, most of the labeled endings in the IC contained small, round vesicles (less than 47 nm in diameter) although a very small number of endings with large, round vesicles also were labeled.(ABSTRACT TRUNCATED AT 400 WORDS)

Auditory cortical projections to the cat inferior colliculus.

The projection from 11 auditory cortical areas onto the subdivisions of the inferior colliculus was studied in adult cats by using two different anterograde tracers to label cortico-collicular (CC) axon terminals. The main results were that: 1) a significant CC projection arose from every field; 2) the principal inferior collicular targets were the dorsal cortex, lateral nucleus, caudal cortex, and intercollicular tegmentum, with only a sparse projection to the central nucleus; 3) the input was usually bilateral, with the ipsilateral side by far the most heavily labeled, and the contralateral projection was a symmetrical subset of the ipsilateral input; 4) the CC system is both divergent and convergent, with single cortical areas projecting to six or more collicular subdivisions, and each auditory midbrain subdivision receiving a convergent projection from two to ten cortical areas; 5) cortical areas devoid of tonotopic organization have topographic projections to collicular target nuclei; 6) the heaviest CC projection terminated in the caudal half of the inferior colliculus; and finally, 7) the relative strength of the cortico-collicular labeling was far less than that of the corresponding corticothalamic projection in the same experiments. The CC system is strategically placed to influence both descending and ascending pathways arising in the inferior colliculus. Nuclei that participate in the premotor system, like the inferior collicular subdivisions that project to the pons, receive substantial corticofugal input. Both the dorsal (pericentral) and the lateral (external) nuclei of the inferior colliculus project to parts of the medial geniculate body whose closest auditory affiliations are with non-tonotopic cortical regions involved in higher order auditory perception. The cortico-collicular system may link brainstem and colliculo-thalamic circuits to coordinate premotor and perceptual aspects of hearing.

Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction.

The projections to the inferior colliculus of the cat are shown in autoradiographs after injections of 3H-amino acids into the anteroventral cochlear nucleus and anterograde axonal transport. Labeled bands of axons are seen in the central nucleus of the inferior colliculus, parallel to the fibrodendritic laminae, and in layers 3 and 4 of the dorsal cortex. A bilateral projection to the lateral, low-frequency part of the inferior colliculus is observed. In contrast, the more ventromedial, mid- and high-frequency parts receive only a contralateral input. The projections from the cochlear nucleus to both the contralateral midbrain and bilaterally to the superior olivary complex appear to be tonotopically organized. After HRP injections in the inferior colliculus, small numbers of stellate neurons are labeled in the lateral and ventral low-frequency parts of the anteroventral cochlear nucleus on the ipsilateral side. EM autoradiographs show labeled axonal endings from both sides of the anteroventral cochlear nuclei are present in the same proportion in pars lateralis. Axonal endings from either cochlear nucleus have small, round synaptic vesicles and make asymmetric synaptic contacts on dendrites. Axons from the contralateral side also make axosomatic contacts on large disc-shaped or stellate cells. Neurons from the ipsilateral anteroventral cochlear nucleus apparently make more synaptic endings per cell as compared to neurons from the contralateral side. Together, bilateral inputs from the anteroventral cochlear nucleus can account for a third of the endings with round synaptic vesicles in pars lateralis of the central nucleus. Morphological similarities among the ascending inputs to the inferior colliculus are discussed. Both direct circuits from the cochlear nucleus to the inferior colliculus and indirect circuits via the superior olivary complex or lateral lemniscus may display banding patterns, nucleotopic organization, or differential synaptic organization. The direct inputs from the anteroventral cochlear nucleus to the colliculus may influence binaural interactions which occur in the superior olivary complex. In addition, direct inputs may create new binaural responses in the inferior colliculus that are independent of lower centers.

Distribution of GABAergic neurons and terminals in the auditory system of the barn owl.

Antisera to GAD (glutamic acid decarboxylase) and GABA were used to determine the distribution of GABAergic cells and terminals in the brainstem and midbrain auditory nuclei of the barn owl. The owl processes time and intensity components of the auditory signal in separate pathways, and each pathway has a distinctive pattern of GAD- and GABA-like immunoreactivity. In the time pathway, all the cells of the cochlear nucleus magnocellularis and nucleus laminaris receive perisomatic GABAergic terminals, and small numbers of GABAergic neurons surround both nuclei. The ventral nucleus of the lateral lemniscus (anterior division) contains both immunoreactive terminals and some GABAergic neurons. In the intensity pathway, dense immunoreactive terminals are distributed throughout the cochlear nucleus angularis, which also contains a small number of GABAergic neurons. The superior olive contains two GABAergic cell types and immunoreactive terminals distributed throughout the neuropil. All the neurons of the nucleus of the lateral lemniscus (ventral part) appear to be GABAergic, and this nucleus also contains a moderate number of immunoreactive terminals. Immunoreactive terminals are distributed throughout the neuropil of the ventral nucleus of the lateral lemniscus (posterior division), whereas multipolar and small fusiform GABAergic neurons predominate in the dorsal regions of the nucleus. The time and intensity pathways combine in the inferior colliculus. The central nucleus of the inferior colliculus contains a larger number of fusiform and stellate GABAergic neurons and a dense plexus of immunoreactive terminals, whereas the external nucleus contains slightly fewer immunoreactive cells and terminals. The superficial nucleus contains dense, fine immunoreactive terminals and a small number of GABAergic neurons.

Morphology of GABAergic neurons in the inferior colliculus of the cat.

The goal of the present study was to provide a comprehensive and quantitative description of neurons immunoreactive for gamma-aminobutyric acid (GABA) in the inferior colliculus (IC) of the cat. Neurons were investigated with two different antisera and two different incubation methods. Free-floating frozen or vibratome-cut sections were incubated either with an antiserum to glutamic acid decarboxylase (GAD) or to GABA conjugated to protein with glutaraldehyde. Additional 1.5-microns-thick sections were incubated with the GABA antiserum after embedding and removal of the plastic. Quantitative data were obtained from much of this material. Despite the use of these different antisera and reaction methods, the results obtained were remarkably similar. The results show that GAD- or GABA-positive neurons represent a significant population of cells in the central nucleus of the IC, up to 20% of the neurons. Most of these neurons have large or medium-sized perikarya. In contrast, immunonegative neurons are medium-sized or small. Many GABA-positive neurons had proximal dendrites or somata oriented in parallel to the fibrodendritic laminae of the central nucleus and are presumed to be disc-shaped neurons. Other have an orthogonal orientation and are presumed to be stellate cells. Large GABA-positive neurons form two groups, those with many axosomatic endings and those with few. Collectively, these observations suggest that there are several types of GABAergic neuron in the central nucleus and, by extension, that these may participate in many types of inhibitory circuits.

Neuron types in the central nucleus of the inferior colliculus that project to the medial geniculate body.

At least four neuron types, distinguished on the basis of dendritic and cell body morphology, were labeled in the central nucleus of the inferior colliculus after horseradish peroxidase injections into the medial geniculate body of the cat. Most labeled cells had disc-shaped dendritic fields whose orientation and arrangement into layers were important identifying features. Most labeled cells were small or medium-sized disc-shaped cells with dendritic fields and cell bodies of corresponding size. These cell types appeared to have dispersed Nissl substance and infrequent axosomatic endings. Large disc-shaped cells, identified by their large dendritic fields and somata, were also labeled. These may have had a different Nissl pattern, including both perinuclear cisterns and clumps of granular endoplasmic reticulum, and numerous axosomatic synaptic endings. Stellate cells, which constituted the fourth labeled cell type, were distinguished by their spherical dendritic fields composed of dendrites radiating in all directions, especially across the layers formed by the disc-shaped cells. Stellate cells probably corresponded to neurons with stacks or clumps of granular endoplasmic reticulum, an irregular nuclear envelope, and frequent axosomatic contacts. These results suggest that many of the cell types previously identified in studies using the Golgi method send their axons to the medical geniculate body. The results also raise the possibility that Nissl pattern and dendritic morphology of central nucleus cell types are related. The presence of several types of neurons in the central nucleus with axons ascending to the thalamus may provide a structural basis for some type of parallel information processing in this part of the central auditory system.