Descending inputs to the octopus cell area of the cat cochlear nucleus: an electron microscopic study.

Large, unilateral lesions of the superior olivary complex (SOC) were made in 18 adult cats. Terminal degeneration was studied electron micrsocopically in the octopus cell area (OCA) of the caudal cochlear nuclei both ipsilateral and contralateral to lesions, after 1 to 14 postoperative days. Three synaptic types (OCA types 1, 2, and 3) have been previously described upon octopus cell somas and dendrites and types 1 and 2 identified as cochlear in origin. The present study shows a new synaptic ending (OCA type 4) on small octopus cell dendrites as well as dendrodendritic contacts. Following SOC ablations, type 4 endings degenerated in the OCA ipsilateral to the lesion. In the COA contralateral to the same lesion, however, degeneration was found in type 3 terminals ending upon more proximal octopus cell dendrities and upon somas. Ipsilateral terminal degeneration occurred between two and four postoperative days, was rare by seven days, and was gone by 14 days after these lesions. However, contralateral terminal degeneration was rare until four days, was most abundant after seven days, and was still present after 14 postoperative days. The different synaptic types and time courses of degeneration in the ipsilateral versus the contralateral OCA, suggested that type 4 endings originate from an ipsilateral source, such as the lesioned periolivary region, while type 3 endings originate from the contralateral SOC or from higher contralateral nuclei. Other evidence for these sources and possible functions of these descending inputs are briefly discussed.

The dorsal nucleus of the lateral lemniscus in the cat: neuronal types and their distributions.

The normal population of neurons and their distributions within the dorsal nucleus of the lateral lemniscus were studied in both Nissl-stained celloidin and frozen sections and in Golgi impregnations from brains of mature cats. According to axial measurements of somata in Nissl-stained material, neurons of the dorsal nucleus of the lateral lemniscus (DNLL) were classified by width:length ratio (r) into round (0.80 less than or equal to r less than or equal to 1.0), ovoid (0.65 < r < 0.80), or elongate (r less than or equal to 0.65) types. These same neurons could also be classed by average diameter (Dm) as large (Dm greater than or equal to 22), medium (12.0 less than or equal to Dm < 22.0), or small (Dm < 12.0). A combination of data on ratios (shape) and average diameters (size) provided the following possible categories of Nissl-stained, DNLL neurons: large round (LR), large ovoid (LO), large elongate (LE), medium round (MR), medium ovoid (MO), medium elongate (ME), small round (SR), small ovoid (SQ), and small elongate (SE). Very few small cells were found, however. Quantitative studies of the distributions of cell type within the whole DNLL showed (1) most medium-sized and most LE cells in the caudal third of the DNLL and (2) most LO and LR cells dorsally located in the rostral third of the DNLL. There were progressively more large and more round types along the caudal-to-rostral axis. In Golgi impregnations of the DNLL, all medium and large cell types, but no small cell types (defined in the Nissl study) were found. Golgi material showed (1) subdivisions of the LO class into vertical (LOV) and horizontal (LOH) types, and (2) radiate (MRR) and oriented (MRO) subclasses of MR neurons according to dendritic arbor and cytology, orientation within the DNLL, and axonal morphology. Examples from all classes of large cells (particularly, LE cells) could have ventrally directed axons. These ventrally directed axons might be efferents to the cochlear nucleus, known from our previous work. A strong horizontal orientation of most DNLL cell somata and dendrites, shown in both our Nissl and Golgi material, is discussed in relation to known inputs to the DNLL. Correlations of our morphological findings with limited electrophysiological data on the DNLL are also discussed.

Neuronal types in the deep dorsal cochlear nucleus of the cat: I. Giant neurons.

Large or "giant" neurons (average somatic diameter greater than 22 micron) of the dorsal cochlear nucleus (DCN) have been carefully described in this light (LM) and electron (EM) microscopic study of normal Nissl-stained and Golgi-impregnated cat brain stems. These neurons can be roughly classed by somatic shape (width:length ratio = r) as elongate (r less than 0.65), ovoid (0.65 less than or equal to r less than 0.75), or spherical (0.75 less than or equal to r less than or equal to 1.0) in Nissl-stained sections. However, orientation and location of somata, size, number, and distribution of basal dendrites and other cytological features seen in Nissl material provided five, easily recognized classes of large neurons: elongate bipolar, elongate multipolar, globular, radiate, and oriented multipolar giant cells. Further cytological details of the dendritic tree and axonal morphology of these neurons, observed in rapid Golgi impregnations of cat and kitten brain stems, extended these descriptive categories of giant neurons. These same deep DCN giant cells were identified in thick plastic sections and in subsequent thin sections. Thin sections showed further neuronal distinctions by relative density of somatic and dendritic synaptic inputs. All giant cells have dense synaptic inputs to basal and primary dendrites but only elongate multipolar and radiate giant cell somata have nearly continuous synaptic coverage of somata. Many axodendritic terminals and some axosomatic endings resemble cochlear endings as identified on fusiform cells of the DCN. Nauta preparations after ipsilateral cochlear ablations have confirmed (1) cochlear input to all giant cell types and (2) different patterns of input to each type. Hence, each giant cell type must process incoming auditory signals, but each cell must receive slightly different primary information. Since some giant cells of each type had observable axons heading into the dorsal acoustic stria, they must all carry encoded primary information to higher auditory centers.

Descending projections from the inferior colliculus to the dorsal cochlear nucleus in the cat: an autoradiographic study.

Descending auditory projections from different subdivisions of the inferior colliculus to the dorsal cochlear nucleus were investigated in experiments using the autoradiographic technique. Tritiated leucine injections confined to the pericentral nucleus of the inferior colliculus resulted in the appearance of dense grain clusters distributed over the outer fusiform cell and molecular layers of the ipsilateral dorsal cochlear nucleus. The pattern and distribution of dense grain clusters strongly resembled the central terminals of glomeruli described previously in the dorsal cochlear nucleus. Injections into the dorsal region of the central nucleus of the inferior colliculus led to a more diffuse distribution of grains over the middle and outer fusiform cell layer and over the innermost molecular layer of the dorsal cochlear nucleus on both sides. Dense grain clusters were also evident after these injections but they appeared to result from the concomitant injection into the overlying pericentral nucleus. Finally, injections of tritiated leucine into the ventral region of the central nucleus of the inferior colliculus (which included some cells of the dorsal nucleus of the lateral lemnisus) resulted in the heaviest labelling of the dorsal cochlear nucleus. Grains were distributed perisomatically and peridendritically around fusiform cells of the fusiform cell layer and giant cells of the deep dorsal cochlear nucleus on both sides. The results indicate that the pericentral nucleus and the more dorsal region of the central nucleus of the inferior colliculus establish overlapping connections with the outermost fusiform cell and molecular layers of the dorsal cochlear nucleus. Both sets of connections seem to be made principally with interneurons through glomerular and other inputs to scattered small cells which exist in these laminae. Since cortical and thalamic descending fibers directly innervate only the most dorsal regions of the inferior colliculus, it may be that this region of the tectum selectively mediates activity from these higher auditory centers. Such centers may indirectly influence fusiform cell response properties through collicular inputs to small cells of the dorsal cochlear nucleus that contact fusiform cells. A more substantial and direct projection was shown to arise from the ventral region of the inferior colliculus to innervate both the fusiform and giant cells. As such, the descending connections from the ventral inferior colliculus may be more likely to influence directly the output of both the fusiform and giant cells and, therefore, the projection of auditory information from the dorsal cochlear nucleus to higher levels.

Descending inputs to caudal cochlear nucleus in cats: a horseradish peroxidase (HRP) study.

After HRP injections into the octopus cell area of the cat cochlear nucleus, only periolivary neurons of the superior olivary complex (SOC) reacted. Elongate neurons in the lateral periolivary nuclei (ipsilateral to the injection) and multipolar neurons in ventromedial periolivary regions (contralateral to the injection) contained granules. No neurons in the main SOC nuclei or higher auditory nuclei reacted, despite a wide range of HRP concentrations. Thus, neurons from the SOC to the octopus cell area of the cochlear nucleus seem to be entirely periolivary and not entirely equivalent to neurons providing collaterals to the olivocochlear bundle.

Descending inputs to the cat dorsal cochlear nucleus: an electron microscopic study.

This experimental study provides identification of several types of terminals in the fusiform cell layer (FCL) of the cat dorsal cochlear nucleus (DCN). Eight types of synaptic terminal were defined in control animals. 22 experimental cats were then subjected to unilateral lesions of the superior olivary complex or SOC (Groups I and II), the inferior colliculus or IC (Groups III and IV), or the IC plus the dorsal nucleus of the lateral lemniscus or DNLL (Groups V and VI). After one to 14 days, animals were killed by perfusion-fixation and brain stems prepared for light and electron microscopic study of degeneration. After SOC lesions, the ipsilateral FCL showed degeneration of small (type 2a) endings on small dendritic shafts; the contralateral FCL showed degeneration of larger (type 5) endings mostly on fusiform cell somata and on some primary dendrites. Both sides showed mild degeneration of large, glomerular (type 1a) endings. After small IC lesions, the ipsilateral FCL demonstrated degenerating type 1a glomerular endings but the contralateral FCL showed severe degeneration of type 5a terminals (axodendritic to fusiform cells) and mild degeneration of both glomerular (type 1a) and axosomatic (type 5) endings. Combined IC-DNLL lesions caused extensive degeneration in a pattern similar to that following IC lesions. In addition retrograde degeneration of fusiform cells occurred bilaterally. These studies showed that: (1) type 2a endings originate in the ipsilateral SOC; (2) type 5 endings on fusiform cell bodies originate from the contralateral SOC; (3) type 5a endings on fusiform cell dendrites originate from the contralateral IC; and (4) type 1a glomerular endings probably arise from several sources, including the IC, the SOC and (possibly) the DNLL of both sides.

Neuroanatomical clues to peripheral locomotor control in small crustaceans (Artemia salina).

Brine shrimp (Artemia salina) were prepared for light and electron microscopy at several stages. Immersion-fixed, rapid Golgi impregnations demonstrated two distinct neuronal types in thoracic appendages of mature, freely swimming Artemia. Isolated motor neurons had large cell somas and thick, radiating dendrites at the body wall-limb junction. A long, elaborate axon extended into the limb. Groups of a second type of neuron with smaller somas and very thin, radiating processes occurred in the distal limb near presumably tactile bristles. Thick axons from motor neurons were traced to terminals associated with limb muscle. Both muscle and axon were best seen with Nomarski optics. Motor axons possessed elongate, irregularly shaped boutons en passant and morphologically variable boutons terminaux; the latter included huge endings with knobbed projectiles arising from thick collaterals, or smaller, round boutons from thin collaterals. In addition, a thick unidentified axon coursed longitudinally within the central body wall, sending short collaterals peripherally. The elaborate peripheral neurons described in this Golgi study may be anatomical correlates for the extraordinary coordination of mature brine shrimp. Because Artemia movements resemble those of leech and decapods, which have been studied extensively electrophysiologically, the possibility of similarly elaborate peripheral structures supplementing central control of locomotion in those invertebrates should be considered.

Development of the octopus cell area in the cat ventral cochlear nucleus.

The octopus cell area (OCA) of the posteroventral cochlear nucleus was studied electron microscopically in kittens. The adult OCA, a region of morphologically homogeneous neurons receiving heterotypic synapses from the cochlea, was used to define the mature state. The OCA reaches cytological maturity at three weeks postnatally, after progression through four stages, defined on the basis of octopus cell cytology (including relative numbers of somatic and dendritic filopodia and spines) and the frequency, ultrastructure and location of previously defined synaptic terminals. Octopus cell size was also studied in rapid Golgi impregnations. The OCA from birth through three postnatal days (stage 1) showed small neurons, few identifiable synaptic types, small, mostly unmyelinated axons, mitotic cells and undifferentiated glia. Between the fourth and seventh postnatal days (stage 2) distinct type 1 and type 2 endings appeared and dendrites thickened, expanded peripherally and developed mature spines. During stage 3 (8-19 days) loss of filopodia, increased somatic spicules, larger somas and clearer differentiation of type 1 and type 2 synapses occurred. After three postnatal weeks (stage 4) the OCA contained morphologically mature octopus cell somas, all three synaptic types ending upon somas and thick basal dendrites, and fascicles of myelinated fibers. Although cytologically mature, the OCA at this stage (about 20-35 days) is substantially smaller than the adult OCA. This smaller size will facilitate further study of OCA synaptic organization.