Plasticity of binaural interaction in the cat inferior colliculus

Responses of single neurones in the inferior colliculus (IC) to acoustic interaural intensity difference (IID) were examined in normal, adult cats and in cats that had been reared for 3–4 months, either from birth or as adults, with unilateral ligation of the external meatus. There were significantly fewer units displaying IID sensitivity in either of the ligated groups than there were in the normal group. The loss of IID sensitivity in the ligated animals reflected a diminished inhibitory input from the non-ligated ear.     

Auditory and visual interactions between the superior and inferior colliculi in the ferret

The integration of visual and auditory spatial information is important for building an accurate perception of the external world, but the fundamental mechanisms governing such audiovisual interaction have only partially been resolved. The earliest interface between auditory and visual processing pathways is in the midbrain, where the superior (SC) and inferior colliculi (IC) are reciprocally connected in an audiovisual loop. Here, we investigate the mechanisms of audiovisual interaction in the midbrain by recording neural signals from the SC and IC simultaneously in anesthetized ferrets. Visual stimuli reliably produced band‐limited phase locking of IC local field potentials (LFPs) in two distinct frequency bands: 6–10 and 15–30 Hz. These visual LFP responses co‐localized with robust auditory responses that were characteristic of the IC. Imaginary coherence analysis confirmed that visual responses in the IC were not volume‐conducted signals from the neighboring SC. Visual responses in the IC occurred later than retinally driven superficial SC layers and earlier than deep SC layers that receive indirect visual inputs, suggesting that retinal inputs do not drive visually evoked responses in the IC. In addition, SC and IC recording sites with overlapping visual spatial receptive fields displayed stronger functional connectivity than sites with separate receptive fields, indicating that visual spatial maps are aligned across both midbrain structures. Reciprocal coupling between the IC and SC therefore probably serves the dynamic integration of visual and auditory representations of space.     

Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice

In auditory maps of the primary auditory cortex, neural response properties are arranged in a systematic way over the cortical surface. As in the visual system, such maps may play a critical role in the representation of sounds for perception and cognition. By recording from single neurons in the central nucleus of the inferior colliculus (ICC) of the mouse, we present the first evidence for spatial organizations of parameters of frequency sweeps (sweep speed, upward/downward sweep direction) and of whole-field tone response patterns together with a map of frequency tuning curve shape. The maps of sweep speed, tone response patterns and tuning curve shape are concentrically arranged on frequency band laminae of the ICC with the representation of slow speeds, build up response types and sharp tuning mainly in the centre of a lamina, and all (including high) speeds, phasic response types and broad tuning mainly in the periphery. Representation of sweep direction shows preferences for upward sweeps medially and laterally and downward sweeps mainly centrally in the ICC (either striped or concentric map). These maps are compatible with the idea of a gradient of decreasing inhibition from the centre to the periphery of the ICC and by gradients of intrinsic neuronal properties (onset or sustained responding). The maps in the inferior colliculus compare favourably with corresponding maps in the primary auditory cortex, and we show how the maps of sweep speed and direction selectivity of the primary auditory cortex could be derived from the here-found maps of the inferior colliculus.     

Sources of GABAergic input to the inferior colliculus of the rat

We have studied the GABAergic projections to the inferior colliculus (IC) of the rat by combining the retrograde transport of horseradish peroxidase (HRP) and immunohistochemistry for γ-amino butyric acid (GABA). Medium-sized (0.06–0.14 μl) HRP injections were made in the ventral part of the central nucleus (CNIC), in the dorsal part of the CNIC, in the dorsal cortex (DCIC), and in the external cortex (ECIC) of the IC. Single HRP-labeled and double (HRP-GABA)-labeled neurons were systematically counted in all brainstem auditory nuclei. Our results revealed that the IC receives GABAergic afferent connections from ipsi- and contralateral brainstem auditory nuclei. Most of the contralateral GABAergic input originates in the IC and the dorsal nucleus of the lateral lemniscus (DNLL). The dorsal region of the IC (DCIC and dorsal part of the CNIC) receives connections mostly from its homonimous contralateral region, and the ventral region from the contralateral DNLL. The commissural GABAergic projections originate in a morphologically heterogeneous neuronal population that includes small to medium-sized round and fusiform neurons as well as large and giant neurons. Quantitatively, the ipsilateral ventral nucleus of the lateral lemniscus is the most important source of GABAergic input to the CNIC. In the superior olivary complex, a smaller number of neurons, which lie mainly in the periolivary nuclei, display double labeling. In the contralateral cochlear nuclei, only a few of the retrogradely labeled neurons were GABA immunoreactive. These findings give us more information about the role of GABA in the auditory system, indicating that inhibitory inputs from different ipsi- and contralateral, mono- and binaural auditory brainstem centers converge in the IC. © 1996 Wiley-Liss, Inc.     

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 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.     

EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: a possible source of inhibitory inputs to the inferior colliculus

The fine structure of the projection from the dorsal nucleus of the lateral lemniscus (DNLL) to the inferior colliculus is examined in the cat. Anterograde axonal transport of 3H-leucine and EM autoradiographic techniques are used to label axonal endings from DNLL. The primary finding is that axonal endings from DNLL contain pleomorphic synaptic vesicles and make symmetrical synaptic contacts. This morphology is associated with inhibitory synapses. The projection from DNLL is the source of approximately one-third of the axonal endings with pleomorphic vesicles in the central nucleus of the inferior colliculus. In the contralateral central nucleus, only labeled endings with pleomorphic vesicles are found. By comparison, on the ipsilateral side, both endings with pleomorphic vesicles and, to a lesser degree, endings with round vesicles are labeled. Endings from DNLL are more numerous per unit area on the contralateral side. About half of the labeled axonal endings from DNLL terminate upon small dendrites, and another third terminate upon more proximal dendrites and several types of cell bodies. Many axonal endings form multiple synaptic contacts, sometimes on more than one postsynaptic structure. Sites of termination for axonal endings include dendritic spines and branch points of dendrites. These data support the hypothesis that the DNLL pathway to the inferior colliculus may have an inhibitory function. Previous studies show that DNLL neurons exhibit immunoreactivity to GAD and GABA antibodies. The crossed projection of DNLL to the inferior colliculus forms tonotopically organized bands that terminate as endings with pleomorphic vesicles. These endings may supply GABAergic inputs to the inferior colliculus. Thus, bands from DNLL could provide inhibitory inputs and overlap with bands from other sources that provide excitatory inputs. Overlapping bands may form unique synaptic domains in the inferior colliculus. The uncrossed projections from DNLL may provide the inferior colliculus with a more diffusely organized projection that could include excitatory and inhibitory inputs. Since the DNLL on one side may inhibit the opposite DNLL and the inferior colliculus, the DNLL pathway may regulate ascending inhibition to the midbrain. Presumed inhibitory inputs from DNLL to the inferior colliculus could be involved in binaural information processing and contralateral dominance.     

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 corticocollicular (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 corticocollicular 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 nontonotopic cortical regions involved in higher order auditory perception. The corticocollicular system may link brainstem and colliculothalamic circuits to coordinate premotor and perceptual aspects of hearing. J. Comp. Neurol. 400:147–174, 1998. © 1998 Wiley-Liss, Inc.     

Topology of the central nucleus of the mustache bat's inferior colliculus: correlation of single unit properties and neuronal architecture

The central nucleus of the mustache bat's inferior colliculus was studied in Golgi, Nissl, and fiber stained preparations; the neuronal organization and cytoarchitecture were correlated with the tonotopic maps revealed by single cell recordings. Three divisions of the central nucleus were defined by anatomical and physiological criteria: the anterolateral, medial, and dorsoposterior divisions. In horizontal sections, the anterolateral division has pronounced, semicircular fibrodendritic laminae. The dendritic fields of adjacent neurons form rostro-caudally-oriented laminae related to the tonotopic sequence. The neurons in the medial division are similar in size and arrangement, but here the laminar orientation follows the lateral-to-medial axis, with less curvature. The dorsoposterior division has many small disc-shaped and stellate neurons and a different, somewhat less fully expressed, laminar orientation. Each division has a unique frequency representation and tonotopic organization which conform to the pattern of dendritic orientation. In the anterolateral division, frequencies from about 10 kHz to about 59 kHz are represented, whereas the frequency representation in the medial division ranges from about 65 kHz to 110 kHz, and higher. The dorsoposterior division has an isofrequency organization in which the best frequency is characteristic for each bat, ranging from 60 to 64 kHz and varying by only +/- 300 Hz. This frequency corresponds to the dominant echo frequency of the bat's echolocation signals. We suggest that the dorsoposterior division is a hypertrophied isofrequency lamina, with many neurocytological features comparable to the isofrequency laminae in the central nucleus of other mammals.     

Auditory brainstem of the ferret: sources of projections to the inferior colliculus

The organization of the auditory brainstem in adult, darkly pigmented ferrets was studied by using the retrograde transport of the lectin wheat germ agglutinin-horseradish peroxidase injected into one inferior colliculus. Retrogradely labelled neurons were found bilaterally in every nucleus of the auditory brainstem. The greatest number of labelled neurons was found in the cochlear nuclei contralateral to the injection site, the ipsilateral medial superior olivary nucleus, both lateral superior olivary nuclei, the ipsilateral ventral nucleus of the lateral lemniscus, both dorsal nuclei of the lateral lemniscus, and the contralateral inferior colliculus. Quantitative assessment of the projections from the cochlear nuclei showed that the number of contralaterally projecting neurons exceeded the number of ipsilaterally projecting neurons by about 50 to one. This ratio remained relatively stable over a wide range of volumes of injected lectin, whereas the absolute number of labelled neurons on each side varied by at least twofold for a constant volume of lectin. These results provide basic data on the ferret auditory system and demonstrate quantitatively some properties of the projections between the cochlear nucleus and the inferior colliculus.     

Lagged cells in the inferior colliculus of the awake ferret

Neurons in the primary auditory cortex (AI) encode complex features of the spectral content of sound, such as direction selectivity. Recent findings of temporal symmetry in AI predict a specific organization of the subcortical input into the cortex that contributes to the emergence of direction selectivity. We demonstrate two subpopulations of neurons in the central nucleus of the inferior colliculus, which differ in their steady‐state temporal response profile: lagged and non‐lagged. The lagged cells (23%) are shifted in temporal phase with respect to non‐lagged cells, and are characterized by an ‘inhibition first’ and delayed excitation in their spectro‐temporal receptive fields. Non‐lagged cells (77%) have a canonical ‘excitation first’ response. However, we find no difference in the response onset latency to pure tone stimuli between the two subpopulations. Given the homogeneity of tonal response latency, we predict that these lagged cells receive inhibitory input mediated by cortical feedback projections.     

The neuronal architecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain

This study defines anatomical subdivisions in Golgi-impregnated material from the inferior colliculus of the cat. The findings demonstrate that the inferior colliculus consists of a mosaic of morphologically distinct parts of neuropil. Each part is also characterized by a unique set of neuronal types. Each part of the inferior colliculus can be defined as tectal or tegmental on the basis of the fundamental pattern of dendritic branching. The main subdivisions of the auditory tectum are the central nucleus, the cortex, and the paracentral nuclei. The central nucleus is distinguished by its laminated neuropil composed of neurons with disc-shaped dendritic fields oriented in parallel arrays with the lemniscal axons. In contrast, the cortex is identified by its broad layers of loosely woven neuropil, which are orthogonal to those in the central nucleus and lack neurons with disc-shaped dendritic fields. The paracentral nuclei, so called because of their scattered arrangement around the central nucleus, are the commissural, dorsomedial, rostral pole, lateral, and ventrolateral nuclei. The main subdivisions of the auditory tegmentum are the pericollicular areas, the nucleus of the brachium of the inferior colliculus, and the sagulum. The pericollicular areas are intercollicular or subcollicular and separate the tectal division from the superior colliculus, central gray, and remaining portions of the tegmentum. The afferent projections to each tectal and tegmental subdivision, as observed in silver-degeneration experiments, distinguish the parcellations based on the Golgi findings. Subdivisions containing tectal cell types receive afferents predominantly from the auditory pathways, in contrast to subdivisions with tegmental cell types, which receive inputs from a wide variety of sources. This suggests a correlation between neuronal types and the nature of their inputs. This analysis of the subdivisions of the inferior colliculus differs from previous studies, especially those relying on Nissl stains. It is likely that subdivisions distinguished by the pattern of the neuropil differ functionally, since the structural components identified in the Golgi-impregnated material are essential parts of the synaptic organization of the auditory midbrain. Future physiological studies should benefit from approaches in which the cell types serve as the focus for the analysis.     

Brief exposure of juvenile rats to noise impairs the development of the response properties of inferior colliculus neurons

Temporary impairment of the auditory periphery during the sensitive period of postnatal development of rats may result in a deterioration of neuronal responsiveness in the central auditory nuclei of adult animals. In this study, juvenile rats (postnatal day 14) were exposed for 8 min to intense broad-band noise; at the age of 3–6 months, the excitatory and inhibitory response areas of neurons in the central nucleus of the inferior colliculus were recorded under ketamine–xylazine anaesthesia in these animals and compared with those of age-matched controls. The response thresholds were similar in the exposed and control animals. The frequency selectivity of low-frequency neurons was comparable in both groups; however, high-frequency neurons had significantly wider excitatory response areas in the exposed rats, indicating disrupted development of high-frequency hearing. Forty-one per cent and 25% of neurons in exposed animals and in controls, respectively, lacked a distinct inhibitory area; these neurons had similar frequency selectivity in the exposed and control rats. As the presence of an inhibitory sideband was associated with sharper frequency tuning in both groups, it appears that lateral inhibition substantially influences neuronal frequency selectivity. If present, the inhibitory areas had comparable bandwidths in both groups; however, they were shifted to the side in the exposed animals, allowing the expansion of the excitatory areas. The results indicate that a brief exposure of juvenile rats to noise leads to a significant worsening of the frequency selectivity of inferior colliculus neurons in adult animals; the poorer frequency selectivity may be due to missing or displaced inhibitory sidebands.     

Intrinsic and commissural connections of the rat inferior colliculus.

This study analyzes the distribution of the intrinsic and commissural fiber plexuses originating in the central nucleus of the inferior colliculus in the rat. The anterograde tracer Phaseolus vulgaris-leucoagglutinin (PHA-L) was injected iontophoretically at different places along the tonotopic axis of the central nucleus and visualized immunohistochemically. In coronal sections the terminal fields of axons originating at each injection site are seen to create four well-defined bands across the rostrocaudal extent of the inferior colliculus, two in the ipsilateral and two in the contralateral side. The "ipsilateral main band" extends dorsomedially and ventrolaterally from the injection site, in register with the known isofrequency contours of the central nucleus, spanning this nucleus and extending into the dorsal cortex of the inferior colliculus. The "ipsilateral external band" is located in the external cortex, where it is oriented dorsoventrally, slightly oblique to the pial surface. In caudal sections, the ventral portion of these two bands appear to join. The two bands in the contralateral inferior colliculus occupy a symmetric position to those of the ipsilateral side, forming a mirror-like image. The position of the four bands changes as the position of the injection site is varied along the frequency gradient axis of the central nucleus. After ventromedial (high frequency area) injections, the main band is ventral and medial, and the external band ventral and lateral. After more dorsolateral (lower frequency) injections, the main band is more dorsal and lateral, whereas the external band is more dorsal but more medial. Thus, the change in the position of the external band is separate and opposite to that of the main band. We suggest that the main bands represent isofrequency contours. Since the projection from the central nucleus to the external cortex of the inferior colliculus also appears to be tonotopic, we also propose a tonotopic organization for the external cortex. The main bands overlap the terminal field of the lemniscal fibers in the central nucleus; thus, it is concluded that the intracollicular fibers contribute to the formation of the known fibrodendritic laminae of the central nucleus. A possible role in preservation of frequency information and integration of other different acoustic parameters is proposed for the main bands. The external bands could participate in polysensory integration, and the commissural connections could be involved in hitherto unknown stages of binaural processing of sound. Based on our results, several modifications are proposed for delineating the subdivisions of the inferior colliculus.     

Auditory nerve fibre responses in the ferret

The ferret (Mustela putorius) is a medium-sized, carnivorous mammal with good low-frequency hearing; it is relatively easy to train, and there is therefore a good body of behavioural data detailing its detection thresholds and localization abilities. However, despite extensive studies of the physiology of the central nervous system of the ferret, even extending to the prefrontal cortex, little is known of the functioning of the auditory periphery. Here, we provide an insight into this peripheral function by detailing responses of single auditory nerve fibres. Our expectation was that the ferret auditory nerve responsiveness would be similar that of its near relative, the cat. However, by comparing a range of variables (the frequency tuning, the variation of rate-level functions with spontaneous rate, and the high-frequency cut-off of phase locking) across several species, we show that the auditory nerve (and hence cochlea) in the ferret is more similar to that of the guinea-pig and chinchilla than to that of the cat. Animal models of hearing are often chosen on the basis of the similarity of their audiogram to that of the human, particularly in the low-frequency region. We show here that whereas the ferret hears well at low frequencies, this is likely to occur via fibres with higher characteristic frequencies. These qualitative differences in response characteristics in auditory nerve fibres are important in interpreting data across all of auditory science, as it has been argued recently that tuning in animals is broader than in humans.     

Cochlear nucleus lesions in the adult gerbil: effects on neurone responses in the contralateral inferior colliculus

Unilateral cochlea ablation in neonatal gerbils has previously been shown to result in transneuronal degeneration of the ventral cochlear nucleus (CN) and enhanced responses of neurones in the contralateral inferior colliculus (IC) to ipsilateral stimulation of the non-ablated ear. Neither effect occurs in adult-ablated animals. To determine whether the lack of physiological change in the adult is due to the persistence of the ventral CN we lesioned the left CN of adult gerbils and recorded neurone responses in the right IC to stimulation of the right ear. Neurone thresholds, latency and intensity/response functions were unaffected by the lesion. The proportion of recording loci in the IC at which excitatory responses were obtained was also unaffected. A transient increase was observed in the maximum unit discharge level. The findings suggest that CN lesions in adults do not produce either the range or degree of neuronal changes resulting from neonatal cochlea ablation and the subsequent transneuronal degeneration of the CN. Thus, the effects of cochlea ablation are age-dependent.     

Effect of background noise on neuronal coding of interaural level difference cues in rat inferior colliculus

Humans can accurately localize sounds even in unfavourable signal‐to‐noise conditions. To investigate the neural mechanisms underlying this, we studied the effect of background wide‐band noise on neural sensitivity to variations in interaural level difference (ILD), the predominant cue for sound localization in azimuth for high‐frequency sounds, at the characteristic frequency of cells in rat inferior colliculus (IC). Binaural noise at high levels generally resulted in suppression of responses (55.8%), but at lower levels resulted in enhancement (34.8%) as well as suppression (30.3%). When recording conditions permitted, we then examined if any binaural noise effects were related to selective noise effects at each of the two ears, which we interpreted in light of well‐known differences in input type (excitation and inhibition) from each ear shaping particular forms of ILD sensitivity in the IC. At high signal‐to‐noise ratios (SNR), in most ILD functions (41%), the effect of background noise appeared to be due to effects on inputs from both ears, while for a large percentage (35.8%) appeared to be accounted for by effects on excitatory input. However, as SNR decreased, change in excitation became the dominant contributor to the change due to binaural background noise (63.6%). These novel findings shed light on the IC neural mechanisms for sound localization in the presence of continuous background noise. They also suggest that some effects of background noise on encoding of sound location reported to be emergent in upstream auditory areas can also be observed at the level of the midbrain.     

Development of the projection from the nucleus of the brachium of the inferior colliculus to the superior colliculus in the ferret

Neurons in the deeper layers of the superior colliculus (SC) have spatially tuned receptive fields that are arranged to form a map of auditory space. The spatial tuning of these neurons emerges gradually in an experience-dependent manner after the onset of hearing, but the relative contributions of peripheral and central factors in this process of maturation are unknown. We have studied the postnatal development of the projection to the ferret SC from the nucleus of the brachium of the inferior colliculus (nBIC), its main source of auditory input, to determine whether the emergence of auditory map topography can be attributed to anatomical rewiring of this projection. The pattern of retrograde labeling produced by injections of fluorescent microspheres in the SC on postnatal day (P) 0 and just after the age of hearing onset (P29), showed that the nBIC-SC projection is topographically organized in the rostrocaudal axis, along which sound azimuth is represented, from birth. Injections of biotinylated dextran amine-fluorescein into the nBIC at different ages (P30, 60, and 90) labeled axons with numerous terminals and en passant boutons throughout the deeper layers of the SC. This labeling covered the entire mediolateral extent of the SC, but, in keeping with the pattern of retrograde labeling following microsphere injections in the SC, was more restricted rostrocaudally. No systematic changes were observed with age. The stability of the nBIC-SC projection over this period suggests that developmental changes in auditory spatial tuning involve other processes, rather than a gross refinement of the projection from the nBIC.     

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 ir 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 electrophysi ological 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 morpholo 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 morpholo 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 centr 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 concentra tions of PL endings come from the ipsilateral lateral superior olive. In combination with inputs from the contralateral dorsal nucleus of the lateral lemniscus, PL endings from the superior olive may participate in many inhibitory synapses found in the central nucleus. These different patterns of synaptic input from the superior olivary complex will influence how binaural information is transmitted to the inferior colliculus. © 1995 Wiley-Liss, Inc.