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A model of auditory thalamic organization is presented incorporating cellular laminae, oriented dendritic arbors and tectothalamic axons as a basis for the tonotopic map at this level of the central auditory system. The heart of this model is the laminar organization of neuronal somata in the ventral division of the medial geniculate body (MGV) of the rabbit, visible in routine Nissl stains. Microelectrode studies have demonstrated a step-wise ascending progression of best frequencies perpendicular to the cell layers. The dendritic arbors of MGV neurons are aligned parallel to the cellular laminae and dendritic tree width along the frequency axis corresponds closely with the frequency steps seen in microelectrode studies. In the laminated subdivision, tectothalamic axons terminate in the form of bands closely aligned with the laminae and dendritic arbors of thalamic relay neurons. The bands of tectothalamic axons extend in the anterior-posterior (A-P) plane forming a dorsal-ventral series of stacked frequency slabs. In the pars ovoidea region, the homologous spiraling of somata, dendritic fields and tectothalamic axons appear to represent a low-frequency area in this species. At least two types of tectothalamic terminals were found within the bands: large boutons frequently arranged in a glomerular pattern and smaller boutons arising from fine caliber axons. We propose that the rabbit is an ideal model to investigate the structural-functional basis of functional maps in the mammalian auditory forebrain.

A laminar organization composed of the dendritic fields of principal neurons and afferent axonal arbors has been proposed as the anatomical substrate for the frequency map at several levels of the mammalian central auditory system, including the inferior colliculus and medial geniculate body (MGB). In contrast to the auditory thalamus in most mammals, the ventral division of the rabbit medial geniculate body (MGV) has cellular laminae visible in routine Nissl stains, allowing a direct comparison of the laminar organization with the dendritic architecture and frequency organization. In total 30 presumptive relay neurons in the MGV were labeled with the juxtacellular recording method, and their dendritic arbors were fully reconstructed from serial sections with the aid of a computer microscope. The spatial organization of MGV dendritic fields was analyzed using the dendritic prism, dendritic stick, and fan-in projection methods. Quantitative spatial analyses revealed that, for MGV neurons in the central pars lateralis subdivision, the major axis of the dendritic fields (approximately 29 degrees relative to the horizontal plane) was closely aligned with that of the Nissl laminae (approximately 25 degrees). Both were oriented orthogonally to the tonotopic axis. In contrast, cells in the pars ovoidea had their major axis of orientation parallel to the anteroposterior axis of the brain. Although a bitufted dendritic field was the norm, it was not uncommon for MGV neurons to have pronounced spatial asymmetries in their dendritic fields. A model is presented that incorporates cellular laminae and oriented dendritic growth to form frequency-related slabs within the MGV., (Copyright 2003 Wiley-Liss, Inc.)

Recent studies have demonstrated that gonadectomy of adult male rats induces dendritic growth of neuroendocrine neurons in the arcuate nucleus. We have hypothesized that these changes are secondary to the loss of testosterone negative feedback. In the present study, we examined the effects of testosterone replacement on the dendritic morphology of arcuate neuroendocrine neurons in castrated rats. Rats were orchidectomized and implanted with silastic capsules designed to produce physiological levels of plasma testosterone (n=9) or empty silastic capsules (n=9) for 2 months. Retrograde labeling with systemically injected Fluoro-Gold, followed by intracellular injection of labeled neurons in a fixed slice preparation, were used to visualize arcuate neuroendocrine neurons. Quantitative analysis of dendritic morphology was performed using three-dimensional computer reconstruction. Serum levels of LH (luteinizing hormone) and testosterone were measured by radioimmunoassay. Treatment of castrated rats with physiological levels of testosterone significantly reduced dendritic length, volume and terminal branch number relative to the castrated rats receiving empty silastic capsules. Dendritic spine density was also greater in the testosterone-treated animals, although the total numbers of spines per dendrite was not significantly different between the two groups. In addition, testosterone replacement was effective in reducing serum LH to levels found in intact rats. These studies demonstrate that testosterone replacement suppresses the dendritic outgrowth of arcuate neuroendocrine neurons that occurs in response to castration. The parallel changes in dendritic arbor and serum LH after castration and hormone replacement suggests that the suppressive effects of testosterone are related to steroid negative feedback.

Recent studies have shown that changes in dendritic architecture are an important component of functional plasticity in the adult central nervous system. In the present study, we determined whether gonadectomy induces changes in dendritic architecture in the arcuate nucleus, a target tissue for gonadal hormones. A combination of retrograde labeling with systemically injected Fluoro-Gold and intracellular injection of neurons in a fixed-slice preparation was used to examine the morphology of neuroendocrine neurons in the rat arcuate nucleus. Intracellullary filled arcuate neuroendocrine neurons (8-21 neurons per brain) from intact (n = 5) and orchidectomized (n = 5) animals were reconstructed with the aid of a computer microscope. A quantitative analysis revealed that orchidectomy had no effect on the number and distribution of Fluoro-Gold-labeled neuroendocrine neurons in the rat arcuate nucleus. The morphology of arcuate neuroendocrine neurons in intact animals was relatively simple, with the majority of neurons (79%) having only two primary dendrites and few dendritic spines. Compared with intact controls, arcuate neuroendocrine neurons in the orchidectomized group had significantly larger somatic profile areas and exhibited significant increases in dendrite length, dendrite volume, terminal branch number, and spines per unit length of dendrite. The increase in terminal branch number in orchidectomized animals was due primarily to the appearance of short branches that gave a striking, claw-like appearance to many of the distal dendrites. These results provide evidence for hormonal regulation of dendritic morphology of arcuate neuroendocrine neurons in adult mammals.

Neonatal rabbits were unilaterally deafened at birth by surgical removal of the stapes, aspiration of the cochlear lymph, and kanamycin injection into the oval window. At 60 days of age, all rabbits were screened with brain stem evoked response tests in order to establish the efficacy of the deafening procedure. The auditory cortex contralateral to the destroyed cochlea was processed according to Golgi-Cox/Nissl procedures. Temporal bone histology revealed nearly complete outer hair cell loss in the damaged cochlea. The dendritic system of lamina III/IV pyramidal neurons contralateral to the deafened ear was digitized from frontal sections using a computer microscope system. Spine counts were also made along the basal dendrites. Spine counts revealed that neonatally deafened rabbits and 38.7% fewer spines along their basal dendrites. No differences between experimental and control rabbits were found in terms of soma cross-sectional area, total number of basal dendrites, total number of dendritic branches and total basal dendritic length. A fan-in projection of the dendritic system revealed no changes in the radial growth of basal dendrites resulting from the early acoustic trauma. In a prior study, spine-free nonpyramidal neurons in the same sections revealed altered dendritic growth and abnormally recurved dendrites. The separate response of pyramidal and nonpyramidal cell types to early cochlear damage is evidence for the different role of epigenetic determinants of dendritic form and orientation in sensory neocortical neurons.

A study of the morphometry and laminar distribution of spine-free nonpyramidal neurons in electrophysiologically verified primary auditory cortex was carried out in adult rabbits. By using image-combining computer microscopy, the locations of all impregnated neurons in 300-micrometers Golgi-Cox Nissl sections through the auditory cortex were determined. Spine-free non-pyramidal neurons constitute nearly 72% of the nonpyramidal neurons present. They are distributed in a band extending from 450 to 750 micrometers beneath the pial surface corresponding to laminae III and IV. A combination of dendritic stick, Fourier, and statistical analyses revealed a highly significant spatial orientation of their dendrite systems along a vertical axis parallel to the apical dendrites of pyramidal neurons. A significant tangential orientation of dendrites along a dorsal-ventral axis was also found. A radial analysis of the dendrite systems revealed that the pronounced vertical orientation of spine-free nonpyramidal neurons is due to (1) directed dendritic growth along the vertical axis, (2) decreased branching and rapid termination of tangentially oriented dendrites, and (3) increased branching of vertically growing dendrites. The radial analysis also revealed that the longest branches are those directed toward the white matter.

We have studied the postnatal development of lamina III/IV spine-free nonpyramidal neurons in the auditory cortex of the New Zealand white rabbit. The morphology and dendritic branching pattern of single cells impregnated with a Golgi-Cox variant were analyzed with the aid of camera lucida drawings and three-dimensional reconstructions obtained with a computer microscope. Sample sizes of 20 neurons were obtained at birth (day 0), postnatal day (PD) 3, 6, 9, 12, 15, 21, and 30 days of age. Normative data were also available from PD-60 and young adult rabbits studied previously. At birth, lamina II-IV have not yet emerged from the cortical plate; immature nonpyramidal neurons at the bottom of the cortical plate (presumptive layer IV) are characterized by short, vertically oriented dendrites. Growth-cone-like structures are present along the shafts and at the tips of the dendrites. At birth, soma area and total dendritic length are, respectively, 34 and 10% of adult values. The cortical plate acquires a trilaminar appearance at PD-3. The six-layered cortex is present by PD-6. During the first postnatal week dendritic length increases fourfold and is accompanied by a significant increase in both terminal and preterminal dendritic growth cones. At the onset of hearing at PD-6, there is a significant proliferation of dendrites and branches to 144 and 200% of adult levels, respectively. These supernumerary dendrites are rapidly lost during the second postnatal week, at which time the somata and dendrites become covered with spines. The loss of higher-order dendrites occurs more gradually; the number of dendritic branches is still 116% of adult values at PD-30. Spine density peaks between days PD-12 and PD-15, and then gradually diminishes until the cells are sparsely spined or spine free by PD-30. Total dendritic length increases in a linear fashion up to PD-15, at which time it is 80% of adult values. An analysis of terminal and intermediate branches demonstrated that the increase in total dendritic length after PD-6 is due entirely to the growth of terminal dendrites. Total dendritic length attains adult levels by PD-30. Spatial analyses revealed that a vertical orientation of dendrites is present at birth. Associated with the onset of hearing at PD-6, there is an explosive elaboration of dendrites toward the pial surface.(ABSTRACT TRUNCATED AT 400 WORDS)

In order to examine the influence of afferent input on nonpyramidal dendrite development in the auditory cortex, unilateral deafening was carried out in neonatal rabbits at birth, approximately 6 days prior to the onset of hearing. Deafening was produced by surgical removal of the incus and stapes ossicles, aspiration of the cochlear perilymph, and kanamycin injection into the oval window. At 60 days of age, acoustic stimulation of the deafened ear was unable to evoke auditory brainstem responses. The brains of experimental and littermate control rabbits were processed according to the Golgi-Cox Nissl method. The dendritic systems of lamina III/IV spine-free nonpyramidal cells in the auditory cortex contralateral to the deafened ear were digitized from 340-micron-thick coronal sections with the aid of a computer microscope. Three-dimensional spatial and statistical analyses revealed that nonpyramidal dendrite length in neonatally deafened rabbits increased 27% relative to littermate controls. A fan-in projection analysis revealed that the increased dendrite length in the deafened animals was maximum in the tangential direction and toward the white matter. Computer rotation of digitized neurons from neonatally deafened rabbits also revealed evidence of abnormal dendritic growth in the form of recurved dendrites. We interpret our results to indicate that unilateral cochlear destruction early in development causes a reorganization of the ascending auditory pathway which extends to the contralateral cerebral cortex. Because the auditory cortex contralateral to the deafened ear still receives acoustic input from the undamaged ipsilateral ear, normal nonpyramidal dendritic growth in the auditory cortex is, in part, dependent upon afferent activity arising from both ears.

The fan-in projection is a computer graphical method of projecting onto a half plane the branching patterns of dendrites and axons that have already been 3-dimensionally digitized. It is suited for neurons possessing an axis of orientation (or elongation), such as cortical neurons. This axis is taken as the polar axis of a spherical coordinate system whose center is the soma. For cortical neurons, the equatorial plane corresponds to the tangential plane. Co-latitude is measured with respect to the positive polar axis. Longitude is discarded. What results is a projection in which dendrites and axons appear to be growing in a half plane whose boundary is the polar axis. The projection eliminates many of the distorting effects of depth foreshortening seen in conventional projections. In so doing it helps one to visualize branching properties that would otherwise be obscure.