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Sources of projections to subdivisions of the inferior colliculus in the rat.

Brainstem and forebrain projections to major subdivisions of the rat inferior colliculus were studied by using retrograde and anterograde transport of horseradish peroxidase. Retrograde label from injection into the external cortex of the inferior colliculus appears bilaterally in cells of the inferior colliculus, as well as in other brainstem auditory groups including the ipsilateral dorsal nucleus of the lateral lemniscus and contralateral dorsal cochlear nucleus. The external cortex is the only collicular subdivision where an injection labels cells in the contralateral cuneate nucleus, gracile nucleus, and spinal trigeminal nucleus. Other projecting cells to the external cortex are found in the lateral nucleus of substantia nigra, the parabrachial region, the deep superior colliculus, the midbrain central gray, the periventricular nucleus, and area 39 of auditory cortex. Injection of the dorsal cortex of inferior colliculus heavily labels pyramidal cells of areas 41, 20, and 36 of the ipsilateral neocortex. Anterograde label from a large injection of auditory cortex is densely distributed in the dorsal cortex, lesser so in the external cortex, and only slightly in the central nucleus. Labelled cells appear in the central nucleus, dorsal cortex, and external cortex, primarily ipsilaterally, following dorsal cortex injection. Relatively few cells from other brainstem auditory groups show projections to the dorsal cortex. Injection of the central nucleus of the inferior colliculus results in robust labelling of nuclei of the ascending auditory pathway including the anteroventral, posteroventral, and dorsal cochlear nuclei (mainly contralaterally), and bilaterally the lateral superior olive, lateral nucleus of the trapezoid body, dorsal nucleus of the lateral lemniscus, and the central nucleus, dorsal cortex, and external cortex of the colliculus. The medial superior olive, superior paraolivary nucleus, and ventral nucleus of the trapezoid body essentially show ipsilateral projections to the central nucleus. The differential distribution of afferents to the inferior colliculus provides a substrate for functional parcellation of collicular subdivisions.

Animals↗

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.

Animals↗

Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat.

The purpose of this study was to identify thalamic areas receiving convergent sensory inputs from acoustic and spinal projection systems in the rat. The topographic distribution of afferents to the thalamus from the inferior colliculus and spinal cord was examined by using WGA-HRP as an anterograde axonal tracer. Following injections in the inferior colliculus, terminal labeling was present in ventral, medial, and dorsal divisions of the medial genicuate body (MGB) and in adjacent areas of the posterior thalamus, including the posterior limitans nucleus, the posterior intralaminar nucleus, the marginal zone, the peripeduncular region, the lateral or parvicellular part of the subparafascicular nucleus, and a region intercalated between the posterior limitans nucleus and the suprageniculate nucleus. In the caudal thalamus spinal projections remained in the reticular formation medial to the collicular terminal field. At intermediate levels of the MG, however, the spinal projection began to overlap the collicular field, terminating in the medial division of the MG and in the posterior intralaminar nucleus, the marginal zone, the lateral subparafascicular nucleus, and the area between the suprageniculate and posterior limitans nuclei. More rostrally, the convergent field expanded to include aspects of the dorsal MG division. The extent to which afferent projections to the thalamus from the inferior colliculus and spinal cord converge is thus graded in the caudorostral plane, with the greatest overlap occurring at the level of the rostral third of the MGB. These observations identify potential areas of acoustic and somesthetic integration and may account for observations of neuronal plasticity in the thalamus in response to the pairing of acoustic and somesthetic inputs.

Afferent Pathways↗

Banding of lateral superior olivary nucleus afferents in the inferior colliculus: a possible substrate for sensory integration.

In this study the organization of the projection from the lateral superior olivary nucleus (LSO) to the inferior colliculus was investigated in the cat by using anterograde tract-tracing techniques. The findings indicated that LSO projected bilaterally to the central nucleus of the inferior colliculus as well as to the ventrolateral and rostral pole nuclei. In the central nucleus a larger medial component of the projection ended in pars medialis and centralis. A smaller lateral component ended in the region of the pars lateralis. Both components of the projection appeared to be topographically organized, but in the lateral component the low-frequency part of LSO appeared to have greater representation. The uncrossed and crossed LSO projections to the inferior colliculus exhibited several important differences in their distribution. First, periodic bands of dense labeling were more prominent in the distribution of the uncrossed projection. The bands measured 150-200 micron in thickness and in some cases interruptions or gaps were present along the length of the bands. The distribution of the crossed projection was more diffuse, but some banding was also apparent. Second, the positions of the bands of dense labeling on the two sides were not homotopic as determined by labeling projections from the ipsilateral and contralateral LSO in the same tissue. The dense bands labeled with WGA-HRP from an injection in LSO on one side and bands labeled with 3H-leucine from an injection in LSO on the other side either were interdigitating or were only partially overlapping. Finally, the area over which the uncrossed projection distributed endings varied in size with respect to that of the crossed projection. The variation in size of the area of the projections was a function of the frequency representation. A model based on the three-dimensional reconstruction of bands as projection sheets is proposed as a substrate for selective integration of afferents in the inferior colliculus.

Afferent Pathways↗

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.

Animals↗

Origin of ascending projections to an isofrequency region of the mustache bat's inferior colliculus.

The inferior colliculus of the mustache bat is similar in most respects to the inferior colliculus of more commonly studied mammals, but one isofrequency contour, the dorsoposterior division, is greatly overrepresented. The present study utilizes this specialization of the auditory system in the mustache bat to determine the total set of ascending projections to a single isofrequency contour of the inferior colliculus. Within the dorsoposterior division, neurons are all very narrowly tuned to 60 kHz, the major component of this bat's echolocation call. The afferent projections to this isofrequency contour were identified by making deposits of horseradish peroxidase (HRP) within the dorsoposterior division after physiologically defining its borders. Two other frequency representations are present in the central nucleus of the inferior colliculus of the mustache bat, the anterolateral division in which there is an orderly progression of frequencies from 59 down to 20 kHz, and the medial division in which frequencies from 63-120 kHz are represented. In additional experiments, the afferent projections to the medial and anterolateral divisions were examined, providing an anatomical description of the tonotopicity of the lower auditory nuclei. Deposits of HRP in the DPD labeled cells in each of the lower brainstem auditory nuclei that have previously been shown to project to the entire central nucleus of the inferior colliculus. The ascending projections to the dorsoposterior division include contralateral projections from the cochlear nucleus and inferior colliculus, ipsilateral projections from the medial superior olive, ventral and intermediate nuclei of the lateral lemniscus, and bilateral projections from the lateral superior olive and dorsal nucleus of the lateral lemniscus. In most of the nuclei, labeled cells were confined to specific portions of the nuclei, often forming "slabs" of labeled cells across the rostrocaudal extent of most nuclei. These slabs presumably represent the 60 kHz representation in each of the lower nuclei. When deposits of HRP were made into other frequency band representations of the inferior colliculus, in either the medial or anterolateral division, labeled cells again formed slabs in each lower nucleus. However, the location of the slab varied as a function of the best frequency of neurons at the deposit site, and labeled cells were not present within the 60 kHz representation. These results show the general tonotopy of the mustache bat's brainstem auditory nuclei, and with respect to the dorsoposterior division, clearly reveal the total set of projections to a single isofrequency region.(ABSTRACT TRUNCATED AT 400 WORDS)

Afferent Pathways↗

Nucleus sagulum: projections of a lateral tegmental area to the inferior colliculus in the cat.

The nucleus sagulum, an area of the midbrain tegmentum, has been considered a component of a lateral tegmental system within the ascending auditory pathway to the thalamus. In this study, connections of the nucleus sagulum within the midbrain were investigated in adult cats. Tracing methods using anterograde and retrograde axonal transport of markers were employed. The nucleus sagulum was identified as a region of principally small neurons (261 +/- 79 micron2) at the margin of the midbrain and neighboring the nuclei of the lateral lemniscus. Injections of tritiated leucine in the nucleus sagulum labeled axons that ended in dense patches within the superficial layers of the caudal portion of the dorsal cortex of the inferior colliculus on the ipsilateral side. Retrograde experiments confirmed this connection. Other axonal projections labeled in the anterograde studies included fibers ending in the dorsomedial nucleus, the superficial layers of the dorsal cortex, and the rostral nucleus of the inferior colliculus with some bilateral distribution. Outside of the inferior colliculus, sagulum injections labeled other axons ending in the ventral intercollicular tegmentum on both sides and in a dorsal and rostral region of the contralateral nucleus sagulum that appeared contiguous with the dorsal nucleus of the lateral lemniscus. The latter region included a population of larger neurons (340-540 micron2) and had different connections with the inferior colliculus. The distribution of axonal labeling after injections in the nucleus sagulum was contrasted with the distribution of projections from several neighboring areas of the lateral tegmentum, including the dorsal nucleus of the lateral lemniscus. None of these areas exhibited connections with the superficial layers of the caudal cortex of the inferior colliculus, which was the major target in the inferior colliculus of the nucleus sagulum. Thus, the results indicated that the nucleus sagulum is distinguished from adjacent regions of the lateral tegmentum by its connectivity. Its association with midbrain auditory pathways is supported by these connections as well as ascending ones to the auditory thalamus.

Animals↗

Auditory brainstem of the ferret: effects of unilateral cochlear lesions on cochlear nucleus volume and projections to the inferior colliculus.

Unilateral lesions of the right cochlea were made in ferrets aged postnatal day (P)12 to P93. The extent of the lesions was assessed by counting remaining hair cells and ganglion cells in midmodiolar sections through the lesioned cochleas and by comparison with a sample of unlesioned cochleas. The neural effects of the lesions were assessed by measuring the volume of each cochlear nucleus (CN) and by counting the number of neurons in each CN that were retrogradely labeled following injections of WGA-HRP in the left inferior colliculus (IC). Survival times between lesioning and injection of the tracer ranged from 11 to 98 days. CN volume and projections to the IC were also measured in a sample of normal adult ferrets and in normal infants aged P39 to P80. Cochlear lesions resulted in a reduction of the volume of the CN on the lesioned side, relative to the other CN, in animals of all ages and survival times. The extent of the CN volume reduction was negatively correlated with the number of remaining cochlear ganglion cells. However, even where the number of ganglion cells was within the normal range, significant volume reductions occurred. The ventral CN was more severely affected by the lesions than the dorsal CN, but no difference was found between the anteroventral and posteroventral divisions of the nucleus. There was no significant difference in the extent of CN volume reductions between animals of different ages or survival times. Lesions of the right cochlea in younger animals (P14 to P24) resulted, after 90 days survival, in an increase in the number of left CN neurons projecting to the left IC. No significant increase was seen following lesions in older (P90) ferrets or following short (11 or 30 days) survival times in young (P14 to P24) ferrets. The extent of the increase in the ipsilateral CN-IC projection was not related to the number of remaining ganglion cells or to the division of the CN examined. Lesions did not affect the contralateral CN-IC projection. We conclude that cochlear lesions in infant ferrets can alter auditory brainstem morphology and connectivity. The dependence of these alterations on the age of the animal, survival time following lesion, and extent of the lesion varies markedly with the index examined.

Animals↗

Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl.

The barn owl determines the directions from which sounds emanate by computing the interaural differences in the timing and intensity of sounds. These cues for sound localization are processed in independent channels originating at nucleus magnocellularis (NM) and nucleus angularis (NA), the cochlear nuclei. The cells of NM are specialized for encoding the phase of sounds in the ipsilateral ear. The cells of NA are specialized for encoding the intensity of sounds in the ipsilateral ear. NM projects solely, bilaterally, and tonotopically to nucleus laminaris (NL). NL and NA project to largely nonoverlapping zones in the central nucleus of the inferior colliculus (ICc), thus forming hodological subdivisions in which time and intensity information may be processed. The terminal field of NL occupies a discrete zone in the rostromedial portion of the contralateral ICc, which we have termed the "core" of ICc. The terminal field of NA surrounds the core of ICc and thus forms a "shell" around it. The projection from NL to the core conserves tonotopy. Low-frequency regions of NL project to the dorsal portions of the core whereas higher-frequency regions project to more ventral portions. This innervation pattern is consistent with earlier physiological studies of tonotopy. Physiological studies have also suggested that NL and the core of ICs contain a representation of the location of a sound source along the horizontal axis. Our data suggest that the projection from NL to the core preserves spatiotopy. Thus, the dorsal portion of NL on the left, which contains a representation of eccentric loci in the right hemifield, innervates the area of the right ICc core that represents eccentric right loci. The more ventral portion of the left NL, which represents loci close to the vertical meridian, innervates the more rostral portions of the right core, which also represents loci near the vertical meridian.

Afferent Pathways↗

Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system?

This study examines the dorsal nucleus of the lateral lemniscus (DNLL) and its afferent and efferent connections. In Nissl-stained material, DNLL has three parts: dorsal, ventral, and lateral. Although each part contains neurons with similar Nissl patterns, the subdivisions may be distinguished by the size, shape, and orientation of the cells. The lateral DNLL contains a mixture of DNLL neurons and cells from the sagulum. Afferent connections to DNLL were investigated with anterograde axonal transport techniques. Bilateral inputs to DNLL arise from the anteroventral cochlear nucleus and lateral superior olive, while unilateral inputs are provided by the ipsilateral medial superior olive and the contralateral DNLL. The inputs appear to have a tonotopic organization. Afferent fibers to DNLL form horizontal bands that are continuous both mediolaterally and rostrocaudally. All parts of DNLL do not share the same inputs, and a medial-to-lateral gradient in the labeling of some pathways is evident. To study the efferent connections of DNLL, both retrograde and anterograde axonal transport techniques were used. The DNLL projects to the inferior colliculus and the contralateral DNLL. The topography of these projections suggests that areas of similar tonotopic organization are connected. In the inferior colliculus, the projection is heaviest to the central nucleus and extends to the adjacent dorsal and caudal cortex, the rostral pole nucleus, and the ventrolateral nucleus. Axons from DNLL terminate along the fibrodendritic laminae of the central nucleus as bands that are prominent on the contralateral side, whereas those on the ipsilateral colliculus are more diffuse. The afferent and efferent connections of DNLL constitute a multisynaptic pathway, parallel to the other ascending pathways to the inferior colliculus. The other ascending pathways include the direct pathways from the cochlear nucleus to the inferior colliculus and the indirect pathways via the superior olivary complex. Ascending pathways are discussed as to their relationship to the subdivisions of the inferior colliculus, the laterality of their projections, and their banding patterns in the central nucleus. In contrast to the excitatory pathways to the inferior colliculus, the neurons in DNLL may use GABA as a neurotransmitter. Axons from the DNLL terminate in the inferior colliculus as bands that could have a unique inhibitory function. Thus, the multisynaptic, DNLL pathway may provide feed-forward inhibitory inputs to the inferior colliculus, bilaterally, and to the contralateral DNLL.

Animals↗

Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance.

Neurons in the lateral superior olive are optimally excited by stimulation of the ipsilateral ear, as are those in the inferior colliculus by stimulation of the contralateral ear. This reversal of ear dominance may result, in part, from distinct crossed excitatory and uncrossed inhibitory pathways ascending from the lateral superior olive. To explore this possibility, immunoreactivity for two putative inhibitory neurotransmitters, glycine and GABA, was examined in projection neurons that retrogradely transported horseradish peroxidase from the cat inferior colliculus. The results suggest that the projection from the lateral superior olive can be segregated, immunocytochemically, into three components: 1) a crossed, glycine-negative (-) projection; 2) an uncrossed, glycine-positive (+) projection; and 3) an uncrossed, glycine(-) projection. Additional evidence suggests that the terminal fields of the two uncrossed projections may distribute differently within the inferior colliculus. Glycine(+) or glycine(-) projection neurons, crossed or uncrossed, do not differ in the size, shape, or location of their somata. However, most glycine(-) neurons are heavily encrusted with glycine(+) endings; glycine(+) neurons have 40-60% fewer of these endings. Glycine(-) neurons located in the lateral limb have fewer glycine (+) perisomatic endings than those in the medial limb. Few projection neurons are GABA(+), and GABA(+) perisomatic endings are rare in the lateral superior olive. Thus, there is a heavy uncrossed projection from the cat lateral superior olive to the inferior colliculus that may be glycinergic and inhibitory. Furthermore, there is a bilateral projection that is not glycinergic or GABAergic, which may be excitatory. The potential contribution of these pathways to contralateral ear dominance in the inferior colliculus is discussed.

Animals↗

Role of commissural projections in the representation of bilateral auditory space in the barn owl's inferior colliculus.

The central nucleus of the barn owl's inferior colliculus (ICc) contains a representation of both the ipsilateral and contralateral auditory hemifields. The representation of ipsilateral space is found in the "core" of the ICc, a subdivision defined by the terminal field of nucleus laminaris, the avian analogue of the medial superior olivary nucleus. The representation of contralateral space is found in the lateral portion of the "shell" of the ICc. The shell surrounds the core and is defined by the terminal field of the nucleus angularis, one of the cochlear nuclei. The representation of ipsilateral space in the core of the ICc may be accounted for by the crossed projection from the nucleus laminaris because most of the nucleus laminaris is devoted to a representation of contralateral space. We present evidence to suggest that the representation of contralateral space is due to a commissural projection from the core of one side to the lateral shell of the opposite side. Injection of horseradish peroxidase (HRP) into the lateral portion of the ICc shell produced retrogradely labeled somata in the core of the opposite side. Injection of tritiated proline into the core produced anterograde label confined to the lateral shell, thus confirming the observations made with HRP. Thus, for example, the left ICc core, which contains predominantly a representation of the left hemifield, innervates the right lateral shell, endowing it with a representation of the left, or contralateral hemifield. The representation of contralateral space in the lateral shell is ultimately conveyed to the external nucleus of the inferior colliculus where it contributes the horizontal axis to a two-dimensional map of space.

Acoustic Stimulation↗

Nigrotectal projection to the inferior colliculus: horseradish peroxidase transport and tyrosine hydroxylase immunohistochemical studies in rats, cats, and bats.

The present study investigated descending projections from the substantia nigra to the auditory tectum. Small (0.02-0.05 microliters) injections of a 30-60% aqueous solution of horseradish peroxidase (HRP) were made unilaterally into the inferior colliculus in rats, cats, and bats (Eptesicus fuscus). Tissue blocks including the substantia nigra, superior colliculus, and inferior colliculus were removed, sectioned, and processed for visualization of HRP. Results show that the substantia nigra, pars lateralis, projects to the inferior colliculus ipsilaterally. In addition, retrogradely labeled cells are found dorsal to the pars lateralis, in a column within the lateral tegmental area of the midbrain. Analysis of injection sites suggests that the principal target of this nigral projection is the dorsal and rostral pericentral region of the inferior colliculus. Immunohistochemical studies with an antibody to tyrosine hydroxylase demonstrate catecholaminergic neurons within the pars lateralis and lateral tegmentum that are similar in location and morphology to one class of HRP retrogradely labeled cells within these structures. These immunohistochemical studies also demonstrate a plexus of fine, varicose tyrosine hydroxylase-positive axons in the rostral pericentral region of the colliculus. The presence of this nigrotectal projection to the inferior colliculus is discussed in relation to its possible role in the control of acousticomotor behavior.

Animals↗

Functional organization of mustached bat inferior colliculus: I. Representation of FM frequency bands important for target ranging revealed by 14C-2-deoxyglucose autoradiography and single unit mapping.

The representation in the inferior colliculus of the frequency modulated (FM) components of the first (25-30 kHz) and second (50-60 kHz) harmonic of the sonar signal of the mustached bat, which may be important for target range processing, was investigated by using the 2-deoxyglucose (2-DG) technique and single-unit mapping. In the 2-DG experiments, bats presented with second harmonic FM stimuli alone showed uptake of label in specific regions of the central nucleus and dorsal cortex of the inferior colliculus, and the nucleus of the brachium. In the central nucleus, a dorsoventrally and mediolaterally elongated slab at the caudal border of the anterolateral division was observed. Labeling in the dorsal cortex was contiguous with this band. Bats stimulated with pairs of first and second harmonic FM stimuli separated by short time delays showed similar patterns of labeling, with the addition of another dorsoventrally elongated region of uptake in the more rostral part of the anterolateral division, associated with label in the dorsal cortex. By comparison to control cases exposed to delayed pairs of first and third harmonic signals, or to a second harmonic constant-frequency tone burst at the bat's reference frequency (ca. 60 kHz), we deduced that this additional region of uptake was attributable to the first harmonic FM component. To elucidate further the details of the tonotopic organization and to correlate the frequency representation with anatomical features of the IC, fine-grained maps of single-unit best frequencies were obtained in the central nucleus. Isofrequency contours were reconstructed by computer from five bats after focal, iontophoretic injection of horseradish peroxidase to locate the penetrations and trace connections of the FM2 area. We found that the tissue volume representing FM2 frequencies (50-60 kHz) showed approximately a sixfold overrepresentation for this frequency band. This region occupied most of the caudal portion of the anterolateral division of the central nucleus. Only a single tonotopic representation was found in the central nucleus, consistent with the pattern seen in other mammals. However, isofrequency contours in the anterolateral division were oriented dorsoventrally, approximately parallel to the coronal plane. The small band of frequencies (ca. 60-62 kHz) associated with the dominant constant-frequency component of the biosonar signal was even more dramatically overrepresented (40x) and was confined to the dorsoposterior division, as previously reported by Zook et al. (1985, 530-456).(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗

Functional organization of mustached bat inferior colliculus: II. Connections of the FM2 region.

Echolocating bats estimate target distance by analyzing the time delay between frequency-modulated portions of their emitted ultrasonic vocalizations and the resultant echoes. In the companion paper we investigated, in the central nucleus of the inferior colliculus, the representation of the predominant second-harmonic frequency-modulated component (FM2) of the mustached bat biosonar signal (O'Neill et al.: J. Comp. Neurol. 283:000-000,'89). In the present paper we report the connections of this part of the colliculus, as determined by focal, iontophoretic injections of HRP following single-unit mapping of the FM2 representation. It was found that the major inputs to the FM2 region of the inferior colliculus come from the contralateral cochlear nucleus; ipsilaterally from the medial superior olive, periolivary nuclei, and ventral and intermediate nuclei of the lateral lemniscus; and bilaterally from the lateral superior olive and dorsal nucleus of the lateral lemniscus. This study identifies for the first time those specific regions of brainstem nuclei providing input to the central nucleus of the inferior colliculus that process FM2 information in the mustached bat. The primary outputs of the FM2 region project to the medial and dorsal divisions of the medial geniculate body. In sharp contrast to other mammals, we found little evidence of connections to the ventral division of the medial geniculate. Other regions receiving significant inputs from the FM2 area include the deep superior colliculus ipsilaterally and the ipsilateral lateral pontine nuclei. Some fibers also terminated near the midline in the dorsal midbrain periaqueductal gray. Sparse intrinsic connections were also seen to the ipsilateral dorsoposterior division of the central nucleus and to the contralateral inferior colliculus at a location homologous to the injection site in the anterolateral division. The finding that FM2 projections to the medial geniculate heavily favor the medial and dorsal divisions is consistent with the location of "FM-FM" delay-dependent facilitation neurons found by Olsen (Processing of Biosonar Information by the Medical Geniculate Body of the Mustached Bat, Pteronotus parnellii. Dissertation, Washington Univ., St. Louis, '86) in these divisions, and with thalamocortical projection patterns in this species. These findings demonstrate that for the FM portions of the biosonar signal, a transformation from a tonotopic form of processing to a more specialized, convergent pattern of organization occurs at the level of the inferior colliculus outputs.

Animals↗

Auditory pathway and auditory activation of primary visual targets in the blind mole rat (Spalax ehrenbergi): I. 2-deoxyglucose study of subcortical centers.

The blind mole rat Spalax ehrenbergi is a subterranean rodent that shows striking behavioral, structural, and physiological adaptations to fossorial life including highly degenerated eyes and optic nerves and a behavioral audiogram that indicates high specialization for low-frequency hearing. A 2-deoxyglucose functional mapping of acoustically activated structures, in conjunction with Nissl/Klüver-Barrera-stained material, revealed a typical mammalian auditory pathway with some indications for specialized low-frequency hearing such as a poorly differentiated lateral nucleus and a well-developed medial nucleus in the superior olive complex. The most striking finding was a marked 2-deoxyglucose labeling of the dorsal lateral geniculate body and of cortical regions that correspond to visual areas in sighted rodents. The results render the blind mole rat a good model system for studying natural neural plasticity and intermodal compensation. In this report, we confine ourselves to the subcortical levels. The cortical level will be dealt comprehensively in a following paper.

Acoustic Stimulation↗

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.

Animals↗

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.

Animals↗