Topographical projection from the superior colliculus to the nucleus of the brachium of the inferior colliculus in the ferret: convergence of visual and auditory information

The normal maturation of the auditory space map in the deeper layers of the ferret superior colliculus (SC) depends on signals provided by the superficial visual layers, but it is unknown where or how these signals influence the developing auditory responses. Here we report that tracer injections in the superficial layers label axons with en passant and terminal boutons, both in the deeper layers of the SC and in their primary source of auditory input, the nucleus of the brachium of the inferior colliculus (nBIC). Electron microscopy confirmed that biocytin-labelled SC axons form axodendritic synapses on nBIC neurons. Injections of biotinylated dextran amine in the nBIC resulted in anterograde labelling in the deeper layers of the SC, as well as retrogradely labelled superficial and deep SC neurons, whose distribution varied systematically with the rostrocaudal placement of the injection sites in the nBIC. Topographical order in the projection from the SC to the ipsilateral nBIC was confirmed using fluorescent microspheres. We demonstrated the existence of functional SC-nBIC connections by making whole-cell current-clamp recordings from young ferret slices. Both monosynaptic and polysynaptic EPSPs were generated by electrical stimulation of either the superficial or deep SC layers. In addition to unimodal auditory units, both visual and bimodal visual-auditory units were recorded in the nBIC in vivo and their incidence was higher in juvenile ferrets than in adults. The SC-nBIC circuit provides a potential means by which visual and other sensory or premotor signals may be delivered to the nBIC to calibrate the representation of auditory space.     

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.     

Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat

We examined the organization of descending projections from the inferior colliculus (IC) to auditory brainstem nuclei and to pontine and reticular nuclei in the rat by employing the anterograde axonal tracer Phaseolus vulgaris-leucoagglutinin (PHA-L). Small PHA-L injections into cytologically defined subnuclei of the IC revealed that each subnucleus has a unique pattern of efferent projections. The central nucleus of the IC projects in a topographic order to the dorsal nucleus of the lateral lemniscus (DLL), the rostral periolivary nucleus (RPO), the ventral nucleus of the trapezoid body (VNTB), and the dorsal cochlear nucleus (DCN). It is assumed that this topography represents a cochleotopic arrangement. The external cortex of the IC projects to the nucleus sagulum (Sag), the RPO, the VNTB, and the DCN. Minor projections were found to pontine and reticular nuclei. Efferent fibers from the dorsal cortex of the IC terminate mainly in the Sag, while other nuclei of the auditory and extra-auditory brainstem receive only minor projections. The intercollicular zone sends a moderate number of fibers to the DLL and very few, if any, to the remaining auditory brainstem nuclei. In contrast, fairly strong projections from the intercollicular zone to the reticular formation were found. The present data demonstrate that the four subnuclei of the IC have a differential pattern of descending projections to nuclei in the pontine and medullary brainstem. These parallel colliculofugal pathways, assumed to belong to functionally separate circuits, may modulate auditory processing at different levels of the auditory neuraxis. © 1993 Wiley-Liss, Inc.     

Patterning of local intracortical projections within the vibrissae representation of rat primary somatosensory cortex

Anterograde and retrograde tracing with biotinylated dextran amine and Phaseolus vulgaris leukoagglutinin was used to assess projection patterns within the vibrissae representation of the rat's primary somatosensorycortex (S-I). Large and small injections of either tracer into the center of the vibrissae representation yielded dense anterograde and retrograde labelling throughout much of the tangential extent of the vibrissae representation within S-I. In all layers, the pattern and extent of retrograde and anterograde label was in rough congruence. The organization of this labelling varied across cortical layers. In layers II and III, labelled fibers extended away from injection sites in all directions and yielded a uniform pattern, which decreased in density with increasing distance from the tracer injection. There was a tendency for labelling to be more extensive along the representation of the row of vibrissae follicles that included the injection site than across rows. There was also a tendency for anterograde labelling to be more extensive in the direction of the representation of follicles more rostral on the face than that injected. In lamina IV, both labelled fibers and cells were restricted for the most part to the septa regions between the barrels. However, a small number of retrogradely labelled neurons were also located in the barrels (approximately one-ninth of the number found in the septa). The pattern observed in laminae II–III was repeated in layers V and VI. In these laminae, there was no evidence of a pattern of intracortical connections related to the vibrissae representation in overlying lamina IV. © 1995 Wiley-Liss, Inc.     

Multiple topographically organized projections connect the central nucleus of the inferior colliculus to the ventral division of the medial geniculate nucleus in the gerbil, Meriones unguiculatus

The ventral division of the medial geniculate nucleus (MGv) receives almost all of its ascending input from the ipsilateral central nucleus of the inferior colliculus (CNIC). In a previous study (Cant and Benson [2006] J. Comp. Neurol. 495:511-528), we made injections of biotinylated dextran amine into the CNIC of the gerbil and demonstrated that it can be divided into two parts. One part (zone 1) receives almost all of its ascending input from the cochlear nuclei, the nuclei of the lateral lemniscus, and the main nuclei of the superior olivary complex; the other part (zone 2) receives inputs from the cochlear nuclei and nuclei of the lateral lemniscus but few or no inputs from the main olivary nuclei. Here we show that these two parts of the CNIC project differentially to the MGv. Axons labeled anterogradely by injections in zone 1 project throughout the rostral two-thirds of the MGv, whereas axons from zone 2 project to the caudal third of the MGv. Throughout much of their extent, the terminal fields do not appear to overlap, although both parts of the CNIC project to medial and dorsal parts of the MGv, and there may be overlap in the most ventral part as well. The results indicate that two parallel pathways arising in the CNIC remain largely separate in the medial geniculate nucleus of the gerbil. It seems most likely that the neurons in the two terminal zones in the MGv perform different functions in audition.     

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.     

Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): differences in distribution of projections from the cochlear nuclei and the superior olivary complex

The inferior colliculus (IC) receives its major ascending input from the cochlear nuclei, the superior olivary complex, and the nuclei of the lateral lemniscus. To understand better the terminal distribution of the inputs from these sources relative to one another, we made focal injections of a retrograde tracer, biotinylated dextran amine, in different parts of the IC in 74 gerbils (Meriones unguiculatus). The cases could be divided into three groups based on counts of labeled cells in brainstem auditory nuclei. Group 1 cases had labeled cells in both the cochlear nuclei and the lateral and medial superior olivary nuclei. Group 2 cases had labeled cells in the cochlear nuclei but few or none in the lateral and medial superior olivary nuclei. Both groups had labeled cells in the nuclei of the lateral lemniscus and the superior paraolivary nucleus. Group 3 cases had few labeled cells in any of the ascending auditory pathways. The group to which a case belonged was strongly related to the location of the injection site in the IC. The injection sites for both group 1 and group 2 were located in the central nucleus, but those for group 1 tended to be located laterally relative to those for group 2, which were located more medially and caudally. The injection sites for group 3 cases lay outside the central nucleus of the IC. The two regions of the central nucleus of the IC, distinguished on the basis of connectivity, are likely to subserve different functions.     

Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum.

The climbing fiber projection to the rat flocculus and adjacent ventral paraflocculus was investigated by using Phaseolus vulgaris-leucoagglutinin as an anterograde and horseradish peroxidase as a retrograde tracer. Large injections of horseradish peroxidase in the flocculus and ventral paraflocculus indicated that the climbing fibers to this region are derived exclusively from any of the following contralateral olivary regions: the dorsal cap of Kooy, the ventrolateral outgrowth, the caudal half of the ventral leaf of the principal olive near its lateral bend, and the rostral pole of the medial accessory olive. Subsequent anterograde and retrograde studies with small injections demonstrated that the latter area projects to the C2 zone, which runs caudally in the ventral paraflocculus and enters the caudal most aspect of the flocculus. The ventral leaf of the principal olive is connected to a D zone in the cerebellar hemisphere and paraflocculus, which, upon entering the ventral paraflocculus, divides into a caudal and rostral strip, termed FD and FD', respectively. The dorsal cap and the ventrolateral outgrowth each project to two distinct zones in the flocculus and part of the ventral paraflocculus. Two floccular zones, which are continuous with the parafloccular FD and FD' zones, receive their climbing fibers from the ventrolateral outgrowth. Two other zones, (FE and FE') receive their climbing fibers from the dorsal cap. The FE' zone is found at the rostral pole of the flocculus and is followed caudalwards by the FD', FE, FD, and C2 zones, respectively. The rostromedial part of the dorsal cap is connected to the continuation of the FE zone into the ventral paraflocculus. The observation that the dorsal cap and the ventrolateral outgrowth are both connected to a set of two alternating zones of floccular/ventral parafloccular Purkinje cells is in agreement with recent studies in the rabbit, and suggests that these zones reflect functionally distinct and discrete units related to specific aspects of visuomotor control.     

Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

Descending projections from the thalamus and related structures to the midbrain are evolutionarily highly conserved. However, the basic organization of this auditory thalamotectal pathway has not yet been characterized. The purpose of this study was to obtain a better understanding of the anatomical and neurochemical features of this pathway. Analysis of the distributions of retrogradely labeled cells after focal injections of retrograde tracer into the inferior colliculus (IC) of the mouse revealed that most of the subcortical descending projections originated in the brachium of the IC and the paralaminar portions of the auditory thalamus. In addition, the vast majority of thalamotectal cells were found to be negative for the calcium‐binding proteins calbindin, parvalbumin, or calretinin. Using two different strains of GAD‐GFP mice, as well as immunostaining for GABA, we found that a subset of neurons in the brachium of the IC is GABAergic, suggesting that part of this descending pathway is inhibitory. Finally, dual retrograde injections into the IC and amygdala plus corpus striatum as well into the IC and auditory cortex did not reveal any double labeling. These data suggest that the thalamocollicular pathway comprises a unique population of thalamic neurons that do not contain typical calcium‐binding proteins and do not project to other paralaminar thalamic forebrain targets, and that a previously undescribed descending GABAergic pathway emanates from the brachium of the IC. J. Comp. Neurol. 525:885–900, 2017. © 2016 Wiley Periodicals, Inc.     

Topography of projections from the auditory cortex to the inferior colliculus in the rat

We examined the organization of descending projections from auditory and adjacent cortical areas to the inferior colliculus (IC) in the rat by using the retrograde and anterograde transport of wheat germ agglutinin-horseradish peroxidase. Small tracer injections were placed into cytologically defined subnuclei of the IC. On the basis of the resulting pattern of retrogradely labeled neurons in the cortex, different cortical areas and fields were defined. Two secondary areas located ventrocaudally (Te2) and ventrally (Te3) to the primary auditory area (Te1) were delineated. The primary auditory area was subdivided into a posterior (Te1.p), a medial (Te1.m), and an anterior (Te1.a) auditory field. In addition, we outlined an area located rostrally to the auditory areas comprising a part of the secondary somatosensory cortex, as well as a dorsal belt surrounding dorsally the auditory areas. The following basic patterns of corticocollicular projections are revealed: 1) layers 2 and 3 of the dorsal cortex of the IC (DC2, DC3) are differentially innervated by the primary auditory fields (Te1.p and Te1.a project bilaterally to DC2, while Te1.m projects bilaterally and in topographical order to DC3); cells in Te1.m, arranged in caudal to rostral sequence, project to corresponding loci in DC3 arranged from dorsolateral to ventromedial; 2) the fibrocellular capsule of the IC, comprising layer 1 of the dorsal and external cortex of the IC, receives input from the secondary auditory area Te2; 3) layers 2 and 3 of the external cortex of the IC are only weakly innervated by the primary and secondary auditory cortex; 4) the intercollicular zone receives its major input from the secondary auditory area Te3, the secondary somatosensory cortex, and the dorsal belt; and 5) finally, the central nucleus of the IC receives no input from the temporal cortex at all. Our results demonstrate that the corticocollicular projections are highly organized. These pathways may modulate auditory processing in different functional circuits of the inferior colliculus.     

Direct comparison of projections from the central amygdaloid region and nucleus accumbens shell

Certain neurochemical and connectional characteristics common to extended amygdala and the nucleus accumbens shell suggest that the two represent a single functional-anatomical continuum. If this is so, it follows that the outputs of the two structures should be substantially similar. To address this, projections from the caudomedial shell and central nucleus of the amygdala, a key extended amygdala structure, were demonstrated in Sprague-Dawley rats with different anterograde axonal tracers processed separately to exhibit distinguishable brown and blue-black precipitates. The caudomedial shell projection is strong in the ventral pallidum and along the medial forebrain bundle through the lateral preopticohypothalamic continuum into the ventral tegmental area, distal to which it thins abruptly. The central nucleus projects strongly to the bed nucleus of the stria terminalis and the sublenticular extended amygdala, but substantially to the lateral hypothalamus only at levels behind the rostral part of the entopeduncular nucleus. Innervation of the ventral tegmental area by the central amygdala is minimal, but the lateral one-third of the substantia nigra, pars compacta and an adjacent lateral part of the retrorubral field receive substantial central amygdala input. Central amygdaloid projections are robust in caudal brainstem sites, such as the reticular formation, parabrachial nucleus, nucleus of the solitary tract and dorsal vagal complex, all of which receive little input from the accumbens. The substantial differences in the output systems of the caudomedial shell of accumbens and central amygdala suggest that the two represent distinct functional-anatomical systems.     

The ventral nucleus of the lateral lemniscus of the gerbil (Meriones unguiculatus): organization of connections with the cochlear nucleus and the inferior colliculus

The spatial organization of projections from the ventral cochlear nucleus (VCN) to the ventral nucleus of the lateral lemniscus (VNLL) and from the VNLL to the central nucleus of the inferior colliculus (CNIC) was investigated by using neuroanatomical tracing methods in the gerbil. In order to label cells in the VNLL that project to the CNIC, focal injections of biotinylated dextran amine (BDA) were made into different CNIC regions. Retrogradely labeled cells were distributed throughout the dorsal-to-ventral axis of the VNLL in all cases. In contrast, the distribution of labeled cells across the lateral-to-medial dimension of the VNLL was related to the location of the injection site along the dorsolateral to ventromedial (frequency) axis of the CNIC. Cells projecting to dorsolateral (low-frequency) regions of the CNIC were located peripherally in the VNLL, mainly laterally and caudally, whereas those projecting to ventromedial (high-frequency) regions of the CNIC tended to be clustered centrally. Projections to the VNLL were labeled anterogradely following injections of BDA in the VCN. The distribution of terminal fields in the VNLL closely paralleled the topographic arrangement of cells projecting to the CNIC; projections from ventrolateral (low-frequency) areas of the VCN terminated mainly along the lateral and caudal borders of the VNLL, whereas projections from dorsomedial (high-frequency) areas terminated in more central regions. The results demonstrate a topographic organization of the major afferent and efferent connections of the gerbil VNLL.     

Organization and origin of the connection from the inferior to the superior colliculi in the rat

The inferior colliculus (IC) is the main ascending auditory relay station prior to the superior colliculus (SC). The morphology and origin of the connection from inferior to superior colliculus (I-SC) was analyzed both by anterograde and retrograde tracing. Irrespective of the subregion of the IC in which they originate, the terminal fields of these connections formed two main tiers in the SC. While the dorsal one primarily involved the stratum opticum and the stratum griseum intermediale, the ventral one innervated the deep strata, although some fibers did connect these tiers. While the dorsal tier occupied almost the whole extension of the SC, the ventral one was mostly confined to its caudomedial quadrant. The fiber density in these tiers decreased gradually in a rostral gradient and the terminal fields became denser as the anterograde tracer at the injection site was distributed more externally in the cortex of the IC. Retrograde tracing confirmed this result, although it did not reveal any topographic ordering for the I-SC pathway. Most presynaptic boutons of the I-SC terminal field were located either inside or close to the patches of acetylcholinesterase activity. Together with previous anatomical and physiological studies, our results indicate that the I-SC connection relays behaviorally relevant information for sensory-motor processing. Our observation that this pathway terminates in regions of the superior colliculus, where neurons involved in fear-like responses are located, reinforce previous suggestions of a role for the IC in generating motor stereotypes that occur during audiogenic seizures.     

Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus

Corticofugal projections to the auditory midbrain, the inferior colliculus (IC), influence the way in which specific sets of IC neurons process acoustic signals. We used retrograde tracer (Fluorogold, Fluororuby, microbeads) injections in the IC to study the morphology and location of cortico-collicular projecting neurons and anterograde tracer (dextran biotin) injections in auditory cortical fields to describe the distribution of terminals in the IC. Nissl staining, cytochrome oxidase activity, and neurofilament SMI32 immunostaining were used to delimit the different auditory areas. We defined a primary or "core" auditory cortex and a secondary "caudal" auditory area containing layer V pyramidal neurons that project to the IC. These projections target the central nucleus of the IC (CNIC) ipsilaterally and the IC cortices bilaterally, with the ipsilateral component predominant. Other secondary auditory areas, dorsal and ventral to the core, do not directly participate in this projection. The ventral secondary cortex targets midbrain periaqueductal gray. The projection from the core cortex originates from two classes of layer V pyramidal cells. Cells presenting a tufted apical dendrite in layer I have dense terminal fields in the IC cortices. Pyramids lacking layer I dendritic tufts target the CNIC in a less dense but tonotopic manner. The caudal cortex projection originates from smaller layer V pyramids and targets the IC cortices with dense terminal fields. Descending auditory inputs from the core and caudal areas converge in the dorsal and external cortices of the IC. Descending connections to the gerbil IC form a segregated system in which multiple descending channels originating from different neuronal subpopulations may modulate specific aspects of ascending auditory information.     

Dorsal nucleus of the lateral lemniscus in the rat: Concentric organization and tonotopic projection to the inferior colliculus

A basic principle of organization in auditory centers is the topographic-tonotopic order. Whether this applies to the dorsal nucleus of the lateral lemniscus (DNLL), however, is still debated. To clarify this problem, we have utilized the neuroanatomical tracers horseradish peroxidase (HRP) and biotinylated dextran (BD) injected into different regions of the central nucleus of the inferior colliculus (CNIC) in the rat. After large injections of HRP that included most of the CNIC, retrogradely labelled neurons were found all across the ipsi- and contralateral DNLL, showing that all parts of this nucleus innervate the CNIC bilaterally. More neurons were seen consistently on the side contralateral to the injection site. Labelled fibers, however, were abundant ipsilaterally, but scarce in the contralateral DNLL. Single, small injections of HRP or BDinto the CNIC resulted in labelling in restricted areas of the ipsi- and contralateral DNLL. In coronal sections, the neurons and fibers labelled in the ipsilateral DNLL formed a well-defined, ring-shaped structure made of dendrites and axons oriented parallel to each other, which we termed “annular band.” The observation of serial sections revealed that the annular band seen in any individual section represents a slice through a more or less complete three-dimensional, hollow, ovoid structure oriented rostrocau-dally. The position and diameter of the annular band changed as the injection site was shifted along the tonotopic axis of the CNIC. Single injections placed in the ventromedial, high-frequency region of the CNIC produced a large annular band along the periphery of the DNLL. After injections placed in progressively more dorsolateral, lower-frequency regions of the CNIC, the annular band became smaller in diameter and occupied a successively more central position in the DNLL. Double injections along the tonotopic axis of the CNIC resulted in two roughly concentric annular bands. The labelled neurons and fibers in the contralateral DNLL systematically occupied a position symmetric to the annular band seen ipsilaterally. These findings indicate that the rat DNLL is primarily composed of neurons with flattened dendritic arbors and flattened fields of terminal fibers. These two elements intermingle, forming concentric layers around the geometric center of the nucleus. The axons of neurons within corresponding layers on the two sides converge onto the CNIC of both sides in a strict topographic fashion: the peripheral layers project to the ventromedial, high-frequency region of the CNIC, and the central layers project to the dorsolateral, low-frequency region. These results suggest that the concentric arrangement of the DNLL is the substrate of its tonotopic organization. © 1994 Wiley-Liss, Inc.     

Efferent connections of the internal globus pallidus in the squirrel monkey: II. topography and synaptic organization of pallidal efferents to the pedunculopontine nucleus

The first objective of the present study was to verify whether projections from regions of the internal pallidum (GPi) that receive inputs from different functional areas of the striatum remain segregated at the level of the pedunculopontine nucleus (PPN) in squirrel monkeys. Second, we analyzed the ultrastructural features and synaptic organization of pallidal terminals in contact with PPN neurons. This was achieved by performing iontophoretic injections of biotinylated dextran amine (BDA) in different regions of the GPi. The animals were pooled into three groups on the basis of the location of the injection sites and the resulting distribution of retrogradely labelled striatal neurons. The experimental groups were divided as follows: group 1: injections in the dorsal one-third of the GPi, retrograde labelling in the head and body of the caudate nucleus (“associative striatum”); group 2: injections in the ventrolateral two-thirds of the GPi, retrograde labelling in the postcommissural region of the putamen (“sensorimotor striatum”); and group 3: injections in the rostromedial pole of the GPi, retrograde labelling in the ventral striatum (“limbic striatum”). These injections led to the anterograde labelling of varicose fibers that arborized profusely in common regions of the PPN dorsal to the brachium conjunctivum. The fields of fibers that arose from the dorsal one-third and the rostromedial pole of the GPi were more widely spread than the afferents from the ventrolateral two-thirds of the GPi. Small numbers of retrogradely labelled cells were encountered in the PPN after each injection in the GPi. Some of them were tightly surrounded by large, BDA-containing varicosities, which implies that the connections between the GPi and the PPN are partly reciprocal. In sections processed for the simultaneous localization of β-nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase (a marker of cholinergic cells in the PPN) and BDA, the anterogradely labelled fibers largely avoided the dense aggregate of NADPH-diaphorase-containing neurons in the PPN pars compacta (PPNc) but, rather, established contacts with unlabelled neurons in the pars dissipata (PPNd). In the electron microscope, the GPi terminals were large (1.0-5.0 μm in diameter), contained many mitochondria and pleomorphic vesicles, and formed symmetric synapses predominantly with proximal dendrites of PPN cells. In conclusion, our data suggest that the noncholinergic neurons of the PPNd are potential targets for the integration of information arising from different functional territories of the GPi in primates. The PPNd is thus in a position to act as an interface between motivational, cognitive, and motor information transmitted along the pallidotegmental projection in primates. J. Comp. Neurol. 382:348-363, 1997. © 1997 Wiley-Liss, Inc.     

Olivocochlear efferent innervation of the organ of corti in hypothyroid rats

Congenital hypothyroidism induces developmental abnormalities in the auditory receptor, causing deafness due to a poor development of the outer hair cells (OHCs) and a lack of synaptogenesis between these cells and the olivocochlear axons. This efferent innervation is formed by two separate systems: the lateral system, which originates in the lateral superior olive (LSO) and reaches the inner hair cells; and the medial system, which originates in the ventral nucleus of the trapezoid body (VNTB) and innervates the OHCs. A previous study carried out in our laboratory showed that in congenitally hypothyroid animals, the neurons which give rise to the efferent system are normal in number and distribution, although smaller in size. The aim of the present work was to study the efferent fibers in the auditory receptor of hypothyroid animals, by means of stereotaxic injections of biotinylated dextran amine in the nuclei that give rise to the olivocochlear system: LSO and VNTB. In hypothyroid animals, injections in LSO gave rise to lateral olivocochlear fibers lacking their characteristic dense terminal arbors, while injections in the VNTB-labeled fibers terminating in the spiral bundle region, far from the OHCs with which they normally contact. In the latter case, only a small percentage of labeled fibers reached the OHCs area, giving off only two radial branches maximum. Because the number of neurons which develop into the efferent innervation was normal in hypothyroid animals, we conclude that medial fibers may contact a new target.     

Structure of intraglomerular dendritic tufts of mitral cells and their contacts with olfactory nerve terminals and calbindin-immunoreactive type 2 periglomerular neurons.

Intraglomerular dendritic tufts of Golgi-impregnated and biotinylated dextran amine (BDA)-labeled mitral cells in the rat main olfactory bulb were analyzed in detail. In particular, the relationships of BDA-labeled tufts with olfactory nerve (ON) terminals and processes of calbindin D-28K-immunoreactive (CB-IR) cells were investigated with confocal laser-scanning light microscopic (CLSM) and electron microscopic (EM) analyses. CB-IR cells were type 2 periglomerular cells that restricted their processes in the ON-free (non-ON) zone of the glomerulus and received few synapses from ON terminals. The mitral tufts varied in complexity, but individual branches were rather simple, smooth processes that bore some branchlets and spines and extended more or less in a straight line or a gentle curve rather than winding tortuously within glomeruli as though they did not consider the compartmental organization, which consisted of ON and non-ON zones that interdigitated in a complex manner with one another. Conventional EM analysis revealed that both thin and thick, presumed proximal branches of mitral/tufted cell dendritic tufts received asymmetrical synapses from ON terminals. Correlated CLSM-EM analysis confirmed direct contacts between the BDA- and CB-labeled processes detected in the CLSM examinations, and synapses were recognized at some of those sites. Furthermore, ON terminals and CB-IR processes were distributed on both proximal and distal dendritic branches in a more or less mosaic pattern. These findings revealed that, on the mitral dendritic tufts, ON terminals and processes of type 2 periglomerular neurons were not clearly segregated proximodistally but, rather, were arranged in a mosaic pattern, which may be important in fine tuning the output from individual glomeruli.     

The projection from striate and extrastriate cortical areas to the superior colliculus in the rat

Following single injections of horseradish peroxidase (HRP) in the superior colliculus (SC) and [3H]proline in the striate cortex of rats, a close correspondence was observed in the topographical arrangements of extrastriate cortical fields of HRP retrograde label and of isotope anterograde label. These results support the notion that extrastriate cortex is divided into multiple physiologically and anatomically defined areas, and they suggest that these areas project separately to SC.