Projections of the nuclei of the lateral lemniscus in the cat: an autoradiographic study

Following injections of [3H]leucine into the dorsal (DLL) and the ventral (VLL) nucleus of the lateral lemniscus in the cat, the efferent projections were studied with the autoradiographic method. Injections into DLL result in heavy labeling in the bilateral inferior colliculus (IC) and the contralateral DLL. Within IC, labeling is dense in the ventrolateral part of the central nucleus (CNv) and moderate in the external nucleus (EN). Labeling in the dorsomedial part of the central nucleus of IC (CNd) is very sparse. All labeled fibers bound for the contralateral side cross in the dorsal part of the midbrain tegmentum at the intercollicular levels via the so-called commissure of Probst. The distribution pattern of labeling in the contralateral IC is almost the same as that in the ipsilateral. In contrast to the cases of injections into DLL, injections into VLL produce labeling in the ipsilateral CNv and EN without labeling in the contralateral IC. A precise comparison of the distribution pattern of labeling within CNv between DLL and VLL injection cases reveals that DLL contributes fibers densely to the dorsal portion of CNv in the proximity of CNd and sparsely to the ventral portion; by contrast, VLL sends many fibers to the ventral portion close to the lateral lemniscus and a few to the dorsal portion. Thus it is suggested that CNv is further divided into dorsal and ventral subdivisions in terms of the terminal zones of afferents from DLL and VLL to CNv. In addition, labeling is found in the medial geniculate body, the nucleus of the trapezoid body and the marginal regions of the superior olivary nuclear complex in both DLL and VLL injection cases, while labeling in the superior colliculus and the pretectum are observed in DLL injection cases only.     

Convergence and divergence of ascending binaural and monaural pathways from the superior olives of the mustached bat

The lateral superior olive and medial superior olive give rise to pathways that terminate in the dorsal nucleus of the lateral lemniscus and central nucleus of the inferior colliculus. In most mammals, neurons in both the medial and lateral superior olives are binaural, but in the mustached bat most neurons in the medial superior olive are monaural. The aims of this study were to determine how the inputs to the medial superior olive contribute to its monaurality and to determine whether the ascending projections from the lateral and medial superior olives overlap or rema in segregated at their targets. Injections of two different tracers were placed in tonotopically matched areas of the lateral and medial superior olives in the same animal. Retrograde transport from injections in the medial superior olive labeled spherical cells in the contralateral anteroventral cochlear nucleus and principal cells in the ipsilateral medial nucleus of the trapezoid body. Few cells were labeled in ipsilateral cochlear nucleus. Anterograde transport resulted in tonotopically specific distributions of label with the same laterality as in nonecholocating mammals. In the dorsal nucleus of the lateral lemniscus, label from the lateral and medial superior olives largely overlapped. In the inferior colliculus, label from the two sources overlapped in the high and low frequency ranges, but in the frequency range around 60 kHz, label from the medial superior olive extended more dorsally than that from the lateral superior olive. These results indicate that projections of the lateral and medial superior olives overlap extensively at their targets. © 1995 Willy-Liss, Inc.     

Two crossed axonal projections contribute to binaural unmasking of frequency-following responses in rat inferior colliculus

Frequency-following responses (FFRs) are sustained potentials based on phase-locked neural activities elicited by low- to medium-frequency periodical sound waveforms. Human brainstem FFRs, which are able to encode some critical acoustic features of speech, can be unmasked by binaural processing. However, the underlying unmasking mechanisms have not previously been reported. In rats, most neurons in the inferior colliculus (IC) exhibit binaural responses which are affected by axonal projections from both the contralateral dorsal nucleus of the lateral lemniscus (DNLL) and the contralateral IC. The present study investigated whether the contralateral DNLL and the contralateral IC modulate binaural unmasking of FFRs recorded in the rat IC. The results show that IC FFRs to the rat pain call (chatter) were enhanced by local injection of the excitatory glutamate receptor antagonist kynurenic acid (KYNA) into the contralateral DNLL but were reduced by KYNA injection into the contralateral IC. Introducing a disparity between the interaural time difference (ITD) of the FFR-eliciting chatter and the ITD of the masking noise enhanced IC FFRs. Moreover, the ITD-disparity-induced FFR enhancement was weakened by injection of KYNA into either the contralateral DNLL or the contralateral IC when the ipsilateral chatter preceded the contralateral chatter. Thus, binaural hearing can improve IC FFRs against noise masking. More importantly, both inhibitory projections from the contralateral DNLL and excitatory projections from the contralateral IC modulate IC FFRs and play a role in forming binaural unmasking of IC FFRs.     

The organization of the lateral thalamus of the hooded rat

Analysis of cytoarchitecture and connectivity showed that the lateral thalamus of the hooded rat is composed of eight nuclei. An examination of the cytoarchitecture permitted the identification of seven cellular fields: nucleus suprageniculatus (sg), nucleus lateralis posterior pars caudomedialis (lpcm), nucleus lateralis posterior pars lateralis (lpl), nucleus lateralis posterior pars rostromedialis (lprm), intramedullary area (ima), nucleus lateralis dorsale pars ventrolateralis (ldvl), and nucleus lateralis dorsale pars dorsomedialis (lddm). An analysis of the connectivity showed that lpl is further divisible into a rostral (lplr) and a caudal (lplc) sector, bringing the total number of nuclei to eight. Nucleus suprageniculatus, the most caudal element of the lateral thalamus, is composed of medium to large, fusiform, and multipolar neurons. It contains a terminal field of the projection of the superficial layers of the ipsilateral superior colliculus. Nucleus lpcm, found rostrolateral to sg, is loosely packed with large multipolar neurons. A terminal field of the superficial layers of the superior colliculus of both sides fits precisely within its cytoarchitectural boundaries. Nucleus lpl, a long cellular territory found lateral to lpcm, extends from the caudal pole of the dorsal lateral geniculate nucleus to the caudal pole of ldvl and contains round cells which are smaller and more densely packed than those of lpcm. Its caudal portion (lplc) contains another terminal field of the ipsilateral superior colliculus while its rostral portion (lplr) contains a terminal field of the projection of Area 17. Area 18 also projects to lplr, whereas Area 18a projects to both lplr and lplc. The intramedullary area, which occupies the fibrous zone between lpl and the dorsal lateral geniculate nucleus, contains round and fusiform neurons and is innervated by Area 18a. Nucleus lprm, situated medial to lpl, is characterized by round neurons which are frequently found in clusters. It is innervated by Areas 17, 18, and 18a. Nucleus ldvl is evenly packed with moderately large, polygonal cells and contains the complete terminal fields of both Areas 17 and 18. It also receives inputs from Area 18a. Finally, lddm, tightly packed with small, round cells and lying medial to ldvl, receives inputs from Area 4.     

The anuran superficial reticular nucleus: evidence for homology with nuclei of the lateral lemniscus

The superficial reticular nucleus (SR) of ranid frogs is part of a lateral cell column extending from the isthmus to the rostral tegmentum. The caudal part of this nucleus receives input from lower brainstem auditory nuclei and projects bilaterally to the torus semicircularis. On the basis of its position, connections, and sensitivity to acoustic stimuli, the caudal SR appears to be homologous to all or part of the mammalian nuclei of the lateral lemniscus.     

Anatomical projections of the nuclei of the lateral lemniscus in the albino rat (rattus norvegicus)

The ascending projections to the lateral lemniscal nuclei and the inferior colliculus were investigated in the albino rat by using Fluoro‐Gold, either alone or in combination with other retrograde tract tracers. Injections were made into the central nucleus of the inferior colliculus (ICC), the dorsal nucleus of the lateral lemniscus (DNLL), the intermediate nucleus of the lateral lemniscus (INLL), or the ventral nucleus of the lateral lemniscus (VNLL). The ICC receives both ipsilateral and contralateral projections from the DNLL and the lateral superior olive, major ipsilateral projections from the INLL, VNLL, medial superior olive, and superior paraolivary nucleus, and major contralateral projections from both dorsal and ventral cochlear nucleus. The DNLL receives a similar pattern of projections from the auditory lower brainstem nuclei. The INLL, in contrast, receives its major projections from the ipsilateral VNLL, lateral superior olive, medial superior olive, superior paraolivary nucleus, and medial nucleus of the trapezoid body, but does not receive a heavy projection from the contralateral lateral superior olive. It receives a major contralateral projection from the ventral cochlear nucleus, but a much lighter projection from the contralateral dorsal cochlear nucleus. The VNLL receives projections from the ipsilateral medial nucleus of the trapezoid body and the contralateral ventral cochlear nucleus, but does not receive projections from the medial or lateral superior olives, the superior paraolivary nucleus, or the dorsal cochlear nucleus. Thus, the three primary subdivisions of the rat's lateral lemniscus can be distinguished from each other on the basis of their distinctive projection patterns. J. Comp. Neurol. 512:573–593, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

Ventral nucleus of the lateral lemniscus in guinea pigs: Cytoarchitecture and inputs from the cochlear nucleus

Cytoarchitectonic criteria were used to distinguish three subdivisions of the ventral nucleus of the lateral lemniscus in guinea pigs. Axonal tracing techniques were used to examine the projections from the cochlear nucleus to each subdivision. Based on the cell types they contain and their patterns of input, we distinguished ventral, dorsal, and anterior subdivisions of the ventral nucleus of the lateral lemniscus. All three subdivisions receive bilateral inputs from the cochlear nucleus, with contralateral inputs greatly outnumbering ipsilateral inputs. However, the relative density of the inputs varies: the ventral subdivision receives the densest projection, whereas the anterior subdivision receives the sparsest projection. Further differences are apparent in the morphology of the afferent axons. Following an injection of Phaseolus vulgaris-leucoagglutinin into the ventral cochlear nucleus, most of the axons on the contralateral side and all of the axons on the ipsilateral side are thin. Thick axons are present only in the ventral subdivision contralateral to the injection site. The evidence from both anterograde and retrograde tracing studies suggests that the thick axons originate from octopus cells, whereas the thin axons arise from multipolar cells and spherical bushy cells. The differences in constituent cell types and in patterns of inputs suggest that each of the three subdivisions of the ventral nucleus of the lateral lemniscus makes a distinct contribution to the analysis of acoustic signals. J. Comp. Neurol. 379:363–385, 1997. © 1997 Wiley-Liss, Inc.     

Differential projection patterns of superior and inferior collicular neurons onto posterior paralaminar nuclei of the thalamus surrounding the medial geniculate body in the rat

The thalamic nuclei at the medial border of the medial geniculate body (i.e. the suprageniculate nucleus, the medial division of the medial geniculate nucleus, the posterior intralaminar nucleus and the peripeduncular nucleus) which relay sensory information to the amygdala are thought to receive convergent input from multiple sites. In order to delineate the organization of these multimodal thalamic nuclei, the locations of superior and inferior collicular neurons projecting to these nuclei were studied by means of retrograde transport methods. Small injections of the tracer Miniruby were made into single paralaminar thalamic nuclei. Injections of Miniruby into the suprageniculate nucleus labelled predominantly neurons in the stratum opticum of the superior colliculus, whereas injections into the medial division of the medial geniculate body, the posterior intralaminar nucleus and the peripeduncular nucleus labelled predominantly neurons in the deep layers of the superior colliculus. These injections also labelled neurons in the inferior colliculus. The majority of retrogradely labelled neurons were found in the external nucleus of the inferior colliculus and here predominantly in layer 2. Injections focused onto the medial division of the medial geniculate body additionally labelled magnocellular neurons in layer 3 of the external nucleus and a few neurons in the central nucleus. More ventrally located injections, focused onto the posterior intralaminar and peripeduncular nucleus, almost exclusively labelled neurons in layer 1 of the external nucleus and the dorsal part of the dorsal nucleus. After injections into the suprageniculate nucleus, only neurons in layer 2 were found. Neurons in the central nucleus of the inferior colliculus were only found after injections that involved the medial division of the medial geniculate body. The present results suggest that, despite a considerable degree of convergence in this thalamic region, each of these thalamic nuclei receives a unique pattern of projections from the superior and inferior colliculi. It appears that the thalamic nuclei may be concerned mainly, but not exclusively, with a single sensory modality, and give rise to parallel multimodal and unimodal pathways to the amygdala.     

Dorsal nucleus of the lateral lemniscus: A nucleus of GABAergic projection neurons

Immunocytochemical staining of the dorsal nucleus of the lateral lemniscus with a well characterized antiserum to glutamate decarboxylase reveals that all, or nearly all, cells in this nucleus show immunoreactivity without the use of agents to block axonal transport. Most somata and dendrites are also contacted by immunoreactive axonal endings. It has previously been established that this nucleus is richly innervated by ascending lemniscal fibers and contains different types of neurons that project to the inferior colliculus. One may conclude that this precollicular nucleus is a major GABAergic feedforward inhibitory center in the acoustic pathway.     

Identification of ventral lateral geniculate nucleus cells projecting to the pretectum and superior colliculus in the cat

Among 235 histologically identified cells of the ventral lateral geniculate nucleus (LGV) in the cat, 66 responded antidromically to electrical stimulation of the pretectum (PT) and/or superior colliculus (SC): 22 projected to PT, 22 to SC and 22 to both sites. The LGV cells were innervated by optic tract fibers corresponding to axons of X- as well as W-type retinal ganglion cells.     

Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus in the rat

The dorsal nucleus of the lateral leminsucs (DLL) is the main source of inhibitory influence in the auditory brainstem of mammals. The cytoarchitecture and connectional properties of DLL were established in the cat in contrast to the rat. The goal of the present study was to establish to what extent the anatomical properties of the rat DLL compare to those of the cat, thus providing a basis of interpretation for future functional studies in the rat, an animal model used more and more in the auditory system. DLL of the rat contains four well-differentiated neuronal types, as seen in Nissl-stained material. Type I neurons are large and multipolar with abundant cytoplasm and darkly stained Nissl substance. Type II neurons are large, bipolar and darkly stained in Nissl material. Type III neurons are medium in size and their soma is round or ovoid. Type IV neurons are small and round with scant cytoplasm; they seem to be also the least common neuronal type of the DLL. After Phaseolus vulgaris-leucoagglutinin or biocytin injections in the DLL, fibers and terminals labeled by orthograde transport were observed in the corresponding region of the contralateral DLL and in the inferior colliculus, bilaterally. A few labeled fibers and terminal fields were seen in the deep layers of the superior colliculus bilaterally, as well as in the medial division of the medial geniculate body and, even more rostrally, in the posterior nucleus of the thalamus. Descending projections from DLL terminated in the periolivary regions of the ipsilateral superior olivary complex. Retrograde tracing based on injections of horseradish peroxidase in the various targets of the DLL confirmed the connections established with orthograde labeling. © 1993 Wiley-Liss, Inc.     

Projections of three subcortical visual centers to marmoset lateral geniculate nucleus

The dorsal lateral geniculate nucleus receives projections from visuotopically organized subcortical nuclei, in addition to inputs from the retina, visual cortices, and the thalamic reticular nucleus. Here, we study subcortical projections to the geniculate from the superior colliculus (SC) and parabigeminal nucleus (PBG) in the midbrain, and the nucleus of the optic tract (NOT) in the pretectum of marmosets. Marmosets are New World diurnal foveate monkeys, and are an increasingly popular model for studying the primate visual system. Furthermore, the koniocellular geniculate layers in marmosets, unlike those in the geniculate of commonly studied diurnal Old World monkeys, are well differentiated from the parvocellular and magnocellular layers. Thus, in the present study, we have made small iontophoretic injections of the retrograde tracer microruby, targeted to the koniocellular layers in the geniculates of four marmosets. We found direct projections from the ipsilateral SC, PBG, and NOT to the koniocellular geniculate layers. The distribution of retrogradely labeled cells in the superficial, visual layers of SC is consistent with the idea that projections from the SC to the koniocellular layers are visuotopically organized. A little over 20 years ago, Vivien Casagrande ( 1994 ) introduced the idea that koniocellular geniculate layers (rather than the parvocellular and magnocellular layers) are principal targets of visuotopically organized subcortical nuclei. Our results add to subsequent evidence assembled by Casagrande and others in favor of this hypothesis.     

Central organization of eighth nerve and mechanosensory lateral line systems in the brainstem of ictalurid catfish

The octavolateral sensory systems in teleost fish comprise at least four distinct hair-cell sensory modalities which are processed separately within the CNS. Two of these modalities, the mechanosensory lateral line system and the eighth nerve auditory system, have been implicated in the animal's ability to detect and localize underwater vibrations. Distinct mechanosensory lateral line and auditory nuclei are present within the torus semicircularis, the midbrain homologue of the inferior colliculus. The present study utilized horseradish peroxidase tracing techniques to delineate those areas of the lower brainstem which are involved in auditory as opposed to mechanosensory lateral line processes. The primary mechanosensory nucleus of the medulla, n. medialis, projects directly to the optic tectum and to the mechanosensory nucleus of the torus semicircularis. Nucleus medialis receives input from primary lateral line nerve fibers as well as from a number of sites within the CNS: n. praeeminentialis pars ventralis, and the eminentia granularis and lobus caudalis of the cerebellum. The n. praeeminentialis itself receives a descending input from the mechanosensory nucleus of the torus semicircularis. These mechanosensory lateral line pathways are parallel to, but distinct from, those of the electrosensory lateral line system. Auditory signals reach the midbrain via an entirely separate route. The octaval nerve terminates in a column of five medullary nuclei. Of these, only the anterior and descending octaval nuclei maintain a direct but sparse projection to the auditory nucleus of the midbrain. The bulk of the auditory input to the midbrain involves a newly described medullary nucleus, the medial auditory nucleus of the medulla. This nucleus receives input from the descending octaval nucleus and projects bilaterally to the auditory nucleus of the torus semicircularis. It is suggested that the medial auditory nucleus of the medulla is homologous to portions of the superior olivary complex of other vertebrates.     

Distribution within the barn owl's inferior colliculus of neurons projecting to the optic tectum and thalamus

Behavioral studies in barn owls indicate that both the optic tectum (OT) and the auditory arcopallium (AAr) mediate sound localization through the presence of neurons that respond only when sound comes from a circumscribed direction in space. The early stages of the computations leading to these so-called space-specific neurons are shared in a common brainstem pathway, which then splits at the level of the inferior colliculus (IC) such that the last computational stage is thought to be duplicated. The study presented here addresses whether the space-specific neurons in OT and AAr are indeed partially independent of each other by using anatomical methods more precise than those used in previous studies. Specifically, projection neurons in IC were retrogradely labelled with injections of fluorescein- and rhodamine-conjugated dextran amines into OT and nucleus ovoidalis (OV), the thalamic nucleus leading to AAr. By labelling the OT-projecting and OV-projecting neurons in the same owl, it was confirmed that neurons in IC project to either OV or OT but not both. However, although a segregation was generally observed between the medially positioned OV-projecting neurons and the laterally positioned OT-projecting neurons, there was also a slight overlap between the two populations. Moreover, electrolytic lesions demarcating physiological tuning properties indicate that many OV-projecting neurons are within the area containing space-specific neurons. These results highlight the need for more detailed studies elucidating the microcircuitry and corresponding physiology of IC, such as have been done in the cortices of the mammalian cerebellum and cerebrum.     

Projections from the superior colliculus to the trigeminal system and facial nucleus in the rat

To determine the influence of the superior colliculus (SC) in orienting behaviors, we examined SC projections to the sensory trigeminal complex, the juxtatrigeminal region, and the facial motor nucleus in rats. Anterograde tracer experiments in the SC demonstrated predominantly contralateral colliculotrigeminal projections. Microinjections in the deep layers of the lateral portion showed labeled nerve fibers and terminals in the ventromedial parts of the caudal principal nucleus and of the rostral oral subnucleus and in the medial part of the interpolar subnucleus. Some terminals were also observed in the juxtatrigeminal region and in the dorsolateral part of the facial motor nucleus contralaterally, overlying the orbicularis oculi motoneuronal region. Verification by retrograde tracer injections into the trigeminal target regions showed labeled SC neurons mostly in lateral portions of layers 4-7. When the juxtatrigeminal region was involved, a remarkable increase of labeled neurons was observed, having a patch-like arrangement with a decreasing gradient from lateral to medial SC portions. Retrograde tracer injections in the dorsolateral VII nucleus showed bilateral labeled neurons mainly in the deep lateral SC portion. Retrograde BDA microinjections into the same trigeminal or juxtatrigeminal regions, followed by gold-HRP into the dorsolateral VII nucleus, demonstrated a significant number of SC neurons in deep layers 6-7 projecting to both structures by axon collaterals. These neurons are mediolaterally grouped in patches along the rostrocaudal SC extent; a subset of them are immunoreactive for glutamic acid decarboxylase (GAD). They could be involved in the coordination of facial movements. Simultaneous anterograde and retrograde tracer injections into the lateral SC portion and the VII nucleus respectively localized trigeminofacial neurons receiving collicular input in the trigeminal principal nucleus and pars oralis. Therefore the SC should play a crucial role in regulating motor programs of both eye and eyelid movements.     

The fine structure of the lateral superior olivary nucleus of the cat

The synaptic organization of the lateral superior olivary nucleus of the cat was analyzed under the electron microscope. The predominant cell type, the fusiform cell, has dendrites that extend from opposite poles of the cell body toward the margins of the nucleus, where they terminate in spinous branches. The fusiform cells are contacted by three types of synaptic terminals that can be distinguished by the size and shape of their synaptic vesicles. The somatic and proximal dendritic surfaces are apposed by synaptic terminals containing small, flat synaptic vesicles. Further from the cell body, the dendrites form numerous synaptic contacts with terminals containing large round vesicles as well as with the terminals containing small, flat vesicles. The most distal dendritic branches and their spiny appendages appear to form synapses almost exclusively with the terminals with large, round vesicles. A relatively rare type of terminal that contains small, round vesicles may form synapses with either the somatic or dendritic surfaces. A few small cells are interspersed among the fusiform cells, but they are more commonly located around the margins of the nucleus. The small cells form few axosomatic contacts. The simplest interpretation of the findings is that the terminals with small, flat vesicles arise in the medial nucleus of the trapezoid body and are inhibitory in function, whereas the terminals with large, round vesicles arise in the anteroventral cochlear nucleus and are excitatory; however, this remains to be demonstrated experimentally. In any case, the differential distribution of these two types of inputs on the somatic and dendritic surfaces must be an important determinant of the physiological response properties of the fusiform cells to binaural acoustic stimuli.