Sources of GABAergic input to the inferior colliculus of the rat

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

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.     

Auditory cortical projections to the cat inferior colliculus

The projection from 11 auditory cortical areas onto the subdivisions of the inferior colliculus was studied in adult cats by using two different anterograde tracers to label corticocollicular (CC) axon terminals. The main results were that: 1) a significant CC projection arose from every field; 2) the principal inferior collicular targets were the dorsal cortex, lateral nucleus, caudal cortex, and intercollicular tegmentum, with only a sparse projection to the central nucleus; 3) the input was usually bilateral, with the ipsilateral side by far the most heavily labeled, and the contralateral projection was a symmetrical subset of the ipsilateral input; 4) the CC system is both divergent and convergent, with single cortical areas projecting to six or more collicular subdivisions, and each auditory midbrain subdivision receiving a convergent projection from two to ten cortical areas; 5) cortical areas devoid of tonotopic organization have topographic projections to collicular target nuclei; 6) the heaviest CC projection terminated in the caudal half of the inferior colliculus; and finally, 7) the relative strength of the corticocollicular labeling was far less than that of the corresponding corticothalamic projection in the same experiments. The CC system is strategically placed to influence both descending and ascending pathways arising in the inferior colliculus. Nuclei that participate in the premotor system, like the inferior collicular subdivisions that project to the pons, receive substantial corticofugal input. Both the dorsal (pericentral) and the lateral (external) nuclei of the inferior colliculus project to parts of the medial geniculate body whose closest auditory affiliations are with nontonotopic cortical regions involved in higher order auditory perception. The corticocollicular system may link brainstem and colliculothalamic circuits to coordinate premotor and perceptual aspects of hearing. J. Comp. Neurol. 400:147–174, 1998. © 1998 Wiley-Liss, Inc.     

Corticofugal modulation of acoustically induced Fos expression in the rat auditory pathway

To investigate the corticofugal modulation of acoustic information ascending through the auditory pathway of the rat, immunohistochemical techniques were used to study the functional expression of Fos protein in neurons. With auditory stimulation at different frequencies, Fos expression in the medial geniculate body (MGB), inferior colliculus (IC), superior olivary complex, and cochlear nucleus was examined, and the extent of Fos expression on the two sides was compared. Strikingly, we found densely Fos-labeled neurons in all divisions of the MGB after both presentation of an auditory stimulus and administration of a gamma-aminobutyric acid type A (GABA(A)) antagonist (bicuculline methobromide; BIM) to the auditory cortex. The location of Fos-labeled neurons in the ventral division (MGv) after acoustic stimulation at different frequencies was in agreement with the known tonotopic organization. That no Fos-labeled neurons were found in the MGv with acoustic stimuli alone suggests that the transmission of ascending thalamocortical information is critically governed by corticofugal modulation. The dorsal (DCIC) and external cortices (ECIC) of the IC ipsilateral to the BIM-injected cortex showed a significantly higher number of Fos-labeled neurons than the contralateral IC. However, no difference in the number of Fos-labeled neurons was found between the central nucleus of the IC on either side, indicating that direct corticofugal modulation occurs only in the ECIC and DCIC. Further investigations are needed to assess the functional implications of the morphological differences observed between the descending corticofugal projections to the thalamus and the IC.     

Transneuronal transport in the vestibular and auditory systems of the squirrel monkey and the arctic ground squirrel. II. Auditory system

Transneuronal transport in the auditory system of the squirrel monkey and the arctic ground squirrel was studied after implantation of tritiated protein or glycoprotein precursors into the ampulla of a single semicircular duct. In both species, essentially the same pattern of transneuronal transport extended beyond the cochlear nuclei to the central nucleus of the inferior colliculus (CNIC), after survival periods ranging from 9 to 33 days. Animals displayed dense labeling over nearly all auditory receptors, nearly all portions of the spiral ganglion and throughout the cochlear nuclei (CN). Labeled fibers, mainly in the ventral acoustic stria, terminated over the ipsilateral lateral superior olive (LSO) and the lateral aspect of medial superior olive (MSO). Fibers continuing medially, decussated in an orderly manner, and terminated over the opposite medial nucleus of the trapezoid body (MNTB) and medial aspect of MSO. Labeled fibers projecting into the opposite lateral lemniscus (LL) terminated in the ventral nucleus of the lateral lemniscus (VNLL) and the CNIC. Fibers, but few terminals, were noted over the dorsal nucleus of the LL. The ipsilateral LL contained comparatively few labeled fibers, but sparse terminations occurred over portions of VNLL and CNIC. No transport of [3H]precursors was noted in the peripheral nuclei of the inferior colliculus or in the medial geneculate body on either side. Massive transport via the contralateral LL and the profuse terminals in the opposite CNIC suggested transneuronal transport via secondary and higher order auditory fibers. Although the largest number of fibers in the contralateral LL probably arose from the cochlear nuclei, higher order fibers also may have arisen from the ipsilateral LSO and the contralateral MSO and VNLL. Small numbers of fibers in both species descended from the region of the superior olivary complex (SOC) ventral to the facial motor nucleus. In the ground squirrel, scant auditory projections were traced into the opposite cochlear nuclei. Tritiated precursors in the endolymph passed most readily from labyrinth to cochlea, and transneuronal transport was more extensive in the auditory pathways than in the vestibular system at comparable times. Centrally transported [3H]fucose was cleared more promptly than [3H]proline in monkeys.     

The topographic organization of corticocollicular projections from physiologically identified loci in the AI,AII, and anterior auditory cortical fields of the cat

The connections of the three auditory fields AI, AII, and the anterior auditory field (AAF) with the inferior colliculus (IC) were studied using anterograde tracing techniques. Microinjections of tracers were placed at physiologically identified loci after these fields had been functionally mapped using microelectrode recording techniques. This methodology ensured that the injections were well within the borders of each cortical field that was studied and enabled the elucidation of the topographies of the projections of AI and AAF onto the IC with respect to their cochleotopicorganizations. The projection of loci in AI to the caudal aspect of the IC was in the form of sheets of terminals in the dorsomedial division of the central nucleus bilaterally and the pericentral nucleus ipsilaterally. The topography of projection with respect to the cochleotopic organization of AI appeared to be in register with the described cochleotopic organization of the central nucleus and the pericentral nucleus. The sheets of labeled terminals in the dorsomedial division of the central nucleus that resulted from the projection of single loci in AI were of the proper orientation to be continuous with the morphological laminae described in the ventrolateral division of the central nucleus. These sheets of corticocollicular terminals also paralleled the dorsomedial aspect of the physiologically defined “isofrequency contours” of the central nucleus. Single injections placed in AAF produced autoradiographic label in the IC that was of the same basic pattern and systematic topography as the labeling recorded with AI injections; however, it was much weaker. The projection from AII was to the lateral (ipsilateral) and medial (bilateral) aspects of the pericentral nucleus.     

Projections of the trapezoid body and the superior olivary complex of the Kangaroo rat (Dipodomys merriami).

Glass micropipettes filled with 2 M sodium cyanide were used to physiologically locate and iontophoretically damage the nucleus of the trapezoid body (NTB), the medial superior olive (MSO), and the lateral superior olive (LSO). Mechanical lesions were made in the trapezoid body as it leaves the cochlear nuclei. After a 3- to 10-day survival time the projections and terminal degeneration were traced with the Fink-Heimer and Nauta-Gygax stains. The ventral cochlear nucleus (VCN) projects via the trapezoid body to ipsilateral LSO, ipsilateral preolivary nuclei, ipsilateral lateral and a contralateral medial dendritic fields of MSO, and contralateral NTB; there is also a small ipsilateral projection to the ventral nucleus of the lateral lemniscus (VNLL) and the central nucleus of the inferior colliculus (CNIC). Some trapezoid body fibers ascend via the contralateral lateral lemniscus to VNLL, DNLL (dorsal nucleus of the lateral lemniscus), and CNIC. There is no projection from the ventral cochlear nucleus to the ipsilateral NTB and contralateral preolivary nuclei. All portions of NTB project ipsilaterally to LSO (ventral NTB to dorsomedial LSO, dorsal NTB to ventral LSO) and to the retro-olivary nucleus. In two animals with NTB lesions there is also degeneration in the ventromedial portion of the ipsilateral facial nucleus. NTB projects contralaterally by way of the stria of Monakow to the pyramidal and molecular cell layers of the dorsal cochlear nucleus (DCN). The NTB does not project ipsilaterally to MSO, preolivary nuclei, VNLL, DNLL and CNIC. Contralaterally there are no projections to any of the nuclei of the auditory pathway except the DCN. Most MSO projections are ipsilateral. The densest goes by way of the lateral lemniscus to the lateral aspect of the ipsilateral CNIC, terminating throughout its dorsoventral axis. MSO also projects bilaterally to the pyramidal and molecular cell layers of dorsal cochlear nucleus (DCN), and ipsilaterally to the ventral portion of the motor nucleus of V and to the facial nucleus. MSO does not project ipsilaterally to the LSO, NTB, preolivary, VCN and retro-olivary nuclei. On the contralateral side, all structures except the DCN are free of projection patterns from axons originating in the MSO. LSO projects bilaterally to the central and ventral portions of CNIC and to the nuclei of the lateral lemnisci, and ipsilaterally to the large and small spherical cell areas of anterior ventral cochlear nucleus (AVCN) and to all portions of DCN. The LSO does not project ipsilaterally to the NTB, MSO, preolivary and retro-olivary nuclei. On the side opposite, this nucleus does not project to NTB, MSO, retro-olive, VCN, preolivary and LSO. For all lesions regardless of the site, there is no degeneration found rostral to the CNIC. The medial geniculate body or other structures in the diencephalon or cortex are free of any fields of terminal degeneration.     

Auditory brainstem projections to the ferret superior colliculus: Anatomical contribution to the neural coding of sound azimuth

The mammalian superior colliculus (SC) contains a neural map of auditory space. It is not known whether this topographic representation emerges at the level of the SC or is relayed there from other auditory areas. We have used retrograde labelling techniques in ferrets to examine the sources and pattern of innervation from auditory brainstem nuclei. After multiple injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the SC, the heaviest concentrations of labelled cells were found in the nucleus of the brachium (BIN) and external nucleus of the inferior colliculus, with much weaker labelling in the nucleus sagulum, dorsal, intermediate and ventral nuclei of the lateral lemniscus, paralemniscal regions, and periolivary nuclei. The projections were predominantly ipsilateral, although labelled cells were found on both sides of the brainstem. Single injections of WGA-HRP or discrete injections of red and green latex microspheres revealed that the caudal and lateral regions of the SC receive the heaviest projections, although the majority of the retrogradely labelled neurons in the contralateral BIN project to rostral SC. On the ipsilateral side, neurons in rostral and caudal regions of the BIN were labelled primarily by the tracer injected into rostral and caudal regions of the SC, respectively. However, no clear segregation was apparent in the BIN after injections into the medial and lateral regions or in any of the other nuclei after either injection paradigm. These data suggest that converging inputs from several auditory brainstem nuclei contribute to the construction of the auditory space map in the SC, although information about sound azimuth may be conveyed to this nucleus via a spatially ordered projection from the ipsilateral BIN. J. Comp. Neurol. 390:342–365, 1998. © 1998 Wiley-Liss, Inc.     

Parabigeminal projections to the superior colliculus in the cat

Small amounts of horseradish peroxidase were injected into the superior colliculus of the cat and the distribution of labeled neurons in the parabigeminal nuclei was mapped. After injections placed dorsal to the stratum opticum in the superior colliculus, the parabigeminal nucleus is the only mesencephalic and/or rhombencephalic structure in which labeled neurons are observed. The number of labeled neurons in the parabigeminal nucleus increases after injections that include both the superficial and the deep layers of the superior colliculus. Each part of the superior colliculus receives projections from wide areas of both parabigeminal nuclei, although it also receives more abundant projections from one or more restricted parts of these nuclei. The anterior third of the parabigeminal nuclei is the part which sends the fewest projections to the superior colliculus. These projections terminate principally in the central and intermediate part of the contralateral colliculus, while a smaller number of fibers terminate in the lateral and rostral part of the ipsilateral colliculus. The intermediate third of the parabigeminal nuclei sends projections to all parts of the ipsilateral colliculus, but the greatest number of these goes to the contralateral colliculus. These contralateral projections terminate principally in the lateral parts of the contralateral colliculus, and in lesser number in its central and rostral, and medial and rostral areas. The posterior third of the parabigeminal nucleus sends scant efferents to wide areas of the ipsilateral and contralateral colliculi, and a dense projection to the medial and intermediate, medial and caudal and central and intermediate parts of the ipsilateral colliculus. There are also consistent projections from the posterior third of the parabigeminal nucleus to the central and rostral and medial and rostral parts of this ipsilateral colliculus. These results demonstrate a topographical organization of the parabigemino-tectal projections in the cat, as a pathway that facilitates the integration in the colliculus of visual impulses of different origin in the retina. This organization permits the modulation of the superior colliculus in its participation in both the extrageniculate visual system and in the regulation of eye and head orientation movements through the parabigeminal projections to the superficial and deep layers of the colliculus, respectively.     

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.     

Focal projections of cat auditory cortex to the pontine nuclei

The pontine nuclei (PN) receive projections from the auditory cortex (AC) and they are a major source of mossy fibers to the cerebellum. However, they have not been studied in detail using sensitive neuroanatomical tracers, and whether all AC areas contribute to the corticopontine (CP) system is unknown. We characterized the projection patterns of 11 AC areas with WGA-HRP. We also compared them with their corticothalamic and corticocollicular counterparts. A third objective was to analyze the structure of the CP axons and their terminals with BDA. Both tracers confirm that all AC areas projected to lateral, central, and medial ipsilateral pontine divisions. The strongest CP projections were from nontonotopic and polymodal association areas. Preterminal fibers formed single terminal fields having many boutons en passant as well as terminal endings, and there was a specific morphological pattern for each pontine target, irrespective of their areal origin. Thus, axons in the medial division had a simpler terminal architecture (type 1 terminal plexus); both the central and lateral pons received more complex endings (type 2 terminal plexus). Auditory CP topographical distribution resembled visual and somatosensory CP projections, which preserve retinotopy and somatotopy in the pons, respectively. However, the absence of pontine tonotopy suggests that the AC projection topography is unrelated to tonotopy. CP input to the medial and central pons coincides with the somatosensory and visual cortical inputs, respectively, and such overlap might subserve convergence in the cerebellum. In contrast, lateral pontine input may be exclusively auditory.     

HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat

The ascending auditory projections to central nucleus of inferior colliculus its ventrolateral and dorsomedial subdivisions (IC_VI, and IC_DM) have been studied in cat using both pressure and electrophoretic injections of horseradish peroxidase (HRP). The results indicate that the predominant ascending projections to inferior colliculus orginate in (1) contralateral cochlear nucleus, (2) contralateral and ipsilateral lateral superior olive, (3) ipsilateral medial superior olive, (4) ipsilateral ventral nucleus of the lateral lemniscus, (5) ipsilateral and contralateral dorsal nucleus of the lateral lemniscus, and (6) contralateral inferior colliculus. In addition, ipsilateral cochlear nucleus, ipsilateral and contralateral intermediate nucleus of the lateral lemniscus, ipsilateral, and to a lesser extent contralateral, periolivary nuclei project to inferior colliculus. Of these nuclei, the lateral superior olive projects exclusively to IC_VL and ipsilateral cochlear nucleus and contralateral inferior colliculus project mostly, if not exclusively, to IC_DM. Many of these projections demonstrate a cochleotopic organization and frequently a nucleotopic organization as well. A cochleotopic organization of the projections is apparent for cochlear nucleus and superior olivary complex. A nucleotopic organization suggests that the heaviest terminations of contralateral inferior colliculus are medial and dorsal in inferior colliculus, of medial superior olive are dorsal and lateral, of superior olivary complex are rostral, of cochlear nucleus are caudal, and of ventral nucleus of the lateral leminiscus are caudal.     

Direct projections to the pretectum and the midbrain reticular formation from auditory relay nuclei in the lower brainstem of the cat

Direct projections to the pretectum and the midbrain reticular formation from auditory relay nuclei in the lower brainstem were examined by the retrograde and anterograde tracer methods in the cat. After horseradish peroxidase (HRP) injection into the pretectomesencephalic reticular region (Pt-MRF), which includes caudoventral regions of the pretectum and rostrodorsal regions of the midbrain reticular formation, labeled neurons were seen in the dorsal nucleus of the lateral lemniscus (DLL), the pericentral (PC) and external (EN) nuclei of the inferior colliculus (IC), the rostral process of IC (RP) and the nucleus of the brachium of IC (NB); no labeled neurons were found in the main laminated portion of the central nucleus of IC. Subsequently, tritiated leucine was injected into DLL, EN, RP or NB for autoradiographic fiber tracing. After injection into DLL or EN, terminal labeling was confined to the ventral portions of the anterior pretectal nucleus. After injection into RP or NB, heavy terminal labeling was observed in the midbrain reticular formation, extending dorsally into the anterior pretectal nucleus. Thus, 3 sectors are distinguishable in Pt-MRF in terms of termination of fibers from the midbrain auditory relay nuclei; the dorsomedial, intermediate or ventrolateral Pt-MRF sector receives fibers arising from DLL, RP or NB, respectively. Fibers from EN terminate only in the dorsal portion (pretectal regions) of the intermediate sector.     

Neocortical projections to the pons and medulla of the nine-banded armadillo (Dasypus novemcinctus)

The pattern of neocortical projections to the pons and medulla was determined by employing the Nauta-Gygax technique ('54) on the brains of armadillos subjected to neocortical ablations. The results of this study indicate that the pretrigeminal basilar pontine gray receives input from a considerable portion of the neocortex. Degenerating fibers resulting from a lesion of the frontal tip of the neocortex terminated within the dorsal medial, the medial and the ventral medial areas of the rostral basilar pontine gray. Corticopontine fibers from the mid-presupraorbital neocortex ended throughout the rostral to caudal extent of the basilar pontine gray, and terminated within the dorsal medial, the medial and the ventral medial areas; whereas degenerating fibers resulting from a lesion of the neocortex immediately rostral to the supraorbital sulcus terminated within the medial, the ventral and the ventral lateral areas of the basilar pontine gray. The neocortex immediately caudal to the supraorbital sulcus distributed corticopontine fibers to the ventral, the ventral lateral, the dorsal lateral and to the dorsal areas of the basilar pontine gray, while degenerating fibers resulting from lesions of the caudal one-third and most caudal tip of the neocortex projected to the ventral and lateral portions of the basilar pontine gray. Neocortical projections to the pontine and medullary reticular formation originated mainly from cortical areas rostral and immediately caudal to the supraorbital sulcus. The neocortex rostral to the supraorbital sulcus distributed to the rostral and medial portions of the pontine reticular formation, whereas corticoreticular fibers from the neocortex immediately caudal to the suprarbital sulcus, also distributed degenerating fascicles to the spinal trigeminal nucleus, the nucleus of the solitary tract and to the nucleus cuneatus. No degenerating fibers were seen to terminate within motor nuclei of cranial nerves located within either the pons or medulla.     

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.     

Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods

Features of the organization of the efferent axonal projections from the medial superior olivary nucleus (MSO) in the cat were studied. In order to determine the origin and distribution of projections from MSO, the retrograde horseradish peroxidase (HRP) and autoradiographic tracing methods were used. The results showed that (1) in both HRP and autoradiographic studies the projection to the inferior colliculus was largely ipsilateral, although a contralateral component was present; (2) the projection field of MSO was confined to the ventral division of the central nucleus of the inferior colliculus, and within this field the labeling was heavier in the rostral and dorsolateral parts of the ventral division; (3) the projection to the inferior colliculus was topographic with ventral parts of MSO projecting ventrally and dorsal parts of MSO projecting dorsolaterally; (4) the projection field in the central nucleus formed successive laminae oriented from ventrolateral to dorsomedial; (5) the axonal course was via the medial or internal segment of the lateral lemniscus; and (6) some fibers in this course ended additionally within the dorsal nucleus of the lateral lemniscus. This latter projection was also topographically organized. These observations supported previously described features of lamination and tonotopic order for afferents of the inferior colliculus, as well as recent suggestions that functional segregation of afferent connections exists within the laminated portion of the central nucleus of the inferior colliculus.     

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.     

Cortical,thalamic, and amygdaloid projections of rat temporal cortex

The cortical, thalamic, and amygdaloid connections of the rodent temporal cortices were investigated by using the anterograde transport of iontophoretically injected biocytin. Injections into area Te1 labeled axons and terminals in the ventral regions of the dorsal and ventral subnuclei of the medial geniculate complex, area Te3, the rostrodorsal part of area Te2, and the ventrocaudal caudate putamen. No amygdaloid labeling was observed. Thalamic projections from Te2 targeted the lateral posterior nucleus, the dorsal part of the dorsal subnucleus of the medial geniculate complex, and the peripeduncular nucleus. Corticocortical projections mainly terminated in the dorsal perirhinal cortex, but moderately dense projections were observed in medial and lateral peristriate cortex, and only light projections were observed to Te1 and Te3. Projections to these isocortical regions terminated in layers I and VI. Amygdaloid projections targeted the ventromedial subdivision of the lateral nucleus and the adjacent part of the anterior basolateral nucleus. Area Te3 was observed to project to the ventrolateral parts of the dorsal and ventral subnuclei of the medial geniculate complex, the dorsal perirhinal cortex, rostral Te2, and Te1. In the amygdala, labeled fibers and terminals were concentrated in the dorsolateral subdivision of the lateral nucleus. These data confirm that areas Te1 and Te3 are hierarchically organized cortical areas connected with auditory relay nuclei in the thalamus. Area Te2, in contrast, appears to be weakly connected with Te1 and Te3 but is heavily connected with the peristriate cortex and tectorecipient thalamic nuclei. Te2 appears to be a visually related cortical area. The data also indicate that projections from Te2 and Te3 target different subregions of the lateral nucleus and that Te2, but not Te3, projects to the basolateral nucleus. J. Comp. Neurol. 382:153-175, 1997. © 1997 Wiley-Liss, Inc.     

Fos expression in GABAergic cells and cells immunopositive for NMDA receptors in the inferior and superior colliculi following audiogenic seizures in rats

Given the evidence that the inferior colliculus (IC) and superior colliculus (SC) seem to play key roles in connecting auditory pathways and seizure output pathways in the neuronal network for audiogenic seizures (AS) in rats, we examined Fos activation in GABAergic cells and cells immunopositive for glutamate N-methyl-D-aspartate (NMDA) receptors in the IC and SC following AS using the double-labeling procedure. Generalized tonic-clonic seizures (GTCS), which developed as an advanced form of AS in some of the susceptible rats, induced an increase in Fos expression in three IC substructures-the dorsal cortex of IC (DCIC), central nucleus of IC (CIC), and external cortex of IC (ECIC)-and in one SC substructure, the deep gray layer of SC (DpG). Compared with the rats showing GTCS, rats exhibiting wild running (WR) without proceeding to GTCS showed a different pattern of AS-induced Fos expression. The DpG in the WR animals showed no significant increase in the levels of Fos-like immunoreactivity. The degrees of Fos activation that occurred in GABAergic cells and cells immunopositive for NMDA receptors were similar in the DCIC, CIC, ECIC, and DpG following AS. These results suggest that Fos activation in the DpG is involved in the development from WR to GTCS in AS-susceptible rats. They also provide some evidence that some GABAergic neurons in the IC and SC and glutamatergic afferents (via NMDA receptors) to these structures are activated by AS.     

Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus

Ascending auditory projections to the inferior colliculus (IC) of the adult gerbil were studied using the retrograde transport of horseradish peroxidase. Our results indicate that in gerbils, the IC receives afferent projections from most brainstem auditory nuclei. A strong contralateral projection originates in the cochlear nuclear complex (CN). A smaller but consistent projection from all three divisions of ipsilateral CN is also present. The medial superior olive (MSO), superior parolivary nucleus, and ventral nucleus of the lateral lemniscus all maintain ipsilateral projections to the IC. Bilateral projections arise from the lateral superior olive, lateral nucleus of the trapezoid body, and dorsal nucleus of the lateral lemniscus. Previous investigations in other mammalian species provide conflicting data concerning the magnitude of a direct ipsilateral projection from CN to the IC. Our quantitative data indicate that the ipsilateral projection from CN in the gerbil is nearly one third as large as the projection from ipsilateral MSO. The projection from contralateral CN is six times larger than the MSO projection. The distribution of labeled cells across the rostrocaudal extent of MSO and the three divisions of the cochlear nuclear complex are presented.