The cytoarchitecture of the nucleus angularis of the barn owl (Tyto alba)

The cochlear nucleus angularis (NA) of the barn owl (Tyto alba) was analyzed using Golgi, Nissl, and tract tracing techniques. NA forms a column of cells in the dorsolateral brainstem that partly overlaps with, and is rostral and lateral to, the cochlear nucleus magnocellularis (NM). Highest best frequencies are mapped in lateral NA (NAl), intermediate in medial NA (NAm), and lowest in the foot region (NAf). Cell density followed the tonotopic axis and decreased with decreasing best frequency. NA contained four major cell classes: planar, radiate, vertical, and stubby. Planar and radiate classes were further subdivided into bipolar and multipolar types according to their number of primary dendrites. Planar neurons were confined to an isofrequency band, whereas radiate neurons had dendrites that could extend across an isofrequency band. Vertical cells had long dendrites oriented perpendicularly to isofrequency bands. Stubby cells were the most numerous and were confined to an isofrequency band because of their short dendrites. Neurons in each of these four classes projected to the inferior colliculus and dorsal nucleus of the lateral lemniscus.     

Subdivisions of the inferior colliculus in the barn owl (Tyto alba)

The inferior colliculus in the barn owl contains three subdivisions: the central (ICC), external (1CX), and superficial (ICS) nuclei. The nuclei are distinguished on the basis of their cyto- and myeloarchitecture, connectivity, and physiological properties. The ICC may be further divided into dorsal (ICCd) and ventral (ICCv) parts. Auditory fibers ascending in the lateral lemniscus enter the ICCd and ICCv, but not the ICX or ICS. The ICX receives its auditory input from the ICC. The ICC and ICX in owls are similar in position, anatomy, connectivity, and physiology to the ICC and ICX in mammals, suggesting that these structures are homologous. Units in the ICC are organized to potopically, whereas units in the ICX are organized according to the locationns of their spatial receptive fields. This implies that a transformation from tonotopic to a spatiotopic organization takes place in the ICX of the owl.     

Development of calretinin immunoreactivity in the brainstem auditory nuclei of the barn owl (Tyto alba).

The early development of calretinin immunoreactivity (CR-IR) was described in the auditory nuclei of the brainstem of the barn owl. CR-IR was first observed in the auditory hindbrain at embryonic day (E17) and a day later (E18) in the inferior colliculus. In each of the auditory nuclei studied, CR-IR did not develop homogeneously, but began in the regions that map high best frequencies in the adult barn owl. In the hindbrain, CR-IR was first observed in the rostromedial regions of the cochlear nucleus magnocellularis and the nucleus laminaris, and in the dorsal regions of the nucleus angularis and in the nucleus of the lateral lemniscus. In the inferior colliculus, CR-IR began in the ventral region of the central core. The edge of these gradients moved along the future tonotopic axes during the development of all nuclei studied, until adult patterns of CR-IR were achieved about a week after hatching.     

Quantitative analysis of the retinal ganglion cell layer and optic nerve of the barn owl Tyto alba

The visual capacity of the common barn owl (Tyto alba) was studied by quantitative analysis of the retina and optic nerve. Cell counts in the ganglion cell layer of the whole-mounted retina revealed a temporal area centralis with peak cell density of 12,500 cells/mm2 and a horizontal streak of high cell density extending from the area centralis into the nasal retina. Integration of the ganglion cell density map gave an estimated total of 1.4 million cells for the ganglion cell layer. Electron microscopy of a single, complete section of the optic nerve revealed a bimodal fiber diameter spectrum (modes at 0.3 and 0.9 microns; bin width = 0.2 microns), with diameters ranging from 0.15 microns (unmyelinated) to 6.05 microns (myelinated, sheath included). The total axon count for the optic nerve was estimated from sample counts to be about 680,000 axons (25% unmyelinated). Therefore, roughly half of the cells in the retinal ganglion cell layer do not send axons into the optic nerve. With certain assumptions, the data predict a visual spatial acuity for barn owls on the order of 8 cycles/degree, a value similar to the known behaviorally measured acuities of masked owls (10 cycles/degree) and domestic cats (6 cycles/degree).     

Adaptation in the auditory midbrain of the barn owl (Tyto alba) induced by tonal double stimulation

During hunting, the barn owl typically listens to several successive sounds as generated, for example, by rustling mice. As auditory cells exhibit adaptive coding, the earlier stimuli may influence the detection of the later stimuli. This situation was mimicked with two double-stimulus paradigms, and adaptation was investigated in neurons of the barn owl's central nucleus of the inferior colliculus. Each double-stimulus paradigm consisted of a first or reference stimulus and a second stimulus (probe). In one paradigm (second level tuning), the probe level was varied, whereas in the other paradigm (inter-stimulus interval tuning), the stimulus interval between the first and second stimulus was changed systematically. Neurons were stimulated with monaural pure tones at the best frequency, while the response was recorded extracellularly. The responses to the probe were significantly reduced when the reference stimulus and probe had the same level and the inter-stimulus interval was short. This indicated response adaptation, which could be compensated for by an increase of the probe level of 5-7 dB over the reference level, if the latter was in the lower half of the dynamic range of a neuron's rate-level function. Recovery from adaptation could be best fitted with a double exponential showing a fast (1.25 ms) and a slow (800 ms) component. These results suggest that neurons in the auditory system show dynamic coding properties to tonal double stimulation that might be relevant for faithful upstream signal propagation. Furthermore, the overall stimulus level of the masker also seems to affect the recovery capabilities of auditory neurons.     

Multiple maps and activity-dependent representational plasticity in the anterior Wulst of the adult barn owl (Tyto alba)

In the present study we addressed the issue of somatosensory representation and plasticity in a nonmammalian species, the barn owl. Multiunit mapping techniques were used to examine the representation of the specialized receptor surface of the claw in the anterior Wulst. We found dual somatotopic mirror image representations of the skin surface of the contralateral claw. In addition, we examined both representations 2 weeks after denervation of the distal skin surface of a single digit. In both representations, the denervated digital representation became responsive to stimulation of the adjacent, mutually functional, digit. The mutability and multiple representations indicates that the Wulst provides the owl with sensory processing capabilities analogous to those in mammals.     

Neural correlates of binaural masking level difference in the inferior colliculus of the barn owl (Tyto alba)

Humans and animals are able to detect signals in noisy environments. Detection improves when the noise and the signal have different interaural phase relationships. The resulting improvement in detection threshold is called the binaural masking level difference. We investigated neural mechanisms underlying the release from masking in the inferior colliculus of barn owls in low‐frequency and high‐frequency neurons. A tone (signal) was presented either with the same interaural time difference as the noise (masker) or at a 180° phase shift as compared with the interaural time difference of the noise. The changes in firing rates induced by the addition of a signal of increasing level while masker level was kept constant was well predicted by the relative responses to the masker and signal alone. In many cases, the response at the highest signal levels was dominated by the response to the signal alone, in spite of a significant response to the masker at low signal levels, suggesting the presence of occlusion. Detection thresholds and binaural masking level differences were widely distributed. The amount of release from masking increased with increasing masker level. Narrowly tuned neurons in the central nucleus of the inferior colliculus had detection thresholds that were lower than or similar to those of broadly tuned neurons in the external nucleus of the inferior colliculus. Broadly tuned neurons exhibited higher masking level differences than narrowband neurons. These data suggest that detection has different spectral requirements from localization.     

The distribution of neurons projecting from the retina and visual cortex to the thalamus and tectum opticum of the barn owl,Tyto alba,and the burrowing owl,Speotyto cunicularia

Using the HRP retrograde transport technique in two different genera of owls (Speotyto and Tyto), we have studied the distribution of neurons projecting to the optic tectum and the visual thalamus. Small injections of HRP were made into these structures from the pial surface after they had been visualized directly by dissection of the overlying bone. In contrast to the findings in mammals, retinal ganglion cells were labeled only in the eye contralateral to the injection site, whether this was in the thalamus or tectum, and the labeled ganglion cells were found on both nasal and temporal sides of the vertical retinal meridian through the fovea. After thalamic injection, labeling was prominent in temporal retina representing the binocular field, temporal to the optic nerve head. Retinothalamic ganglion cells formed roughly concentric lines of isodensity centered on the fovea (Speotyto) or area centralis (Tyto); labeling form thalamic injections involved both large and medium-sized neurons, but did not involve the smallest nor a conspicuous class of very large neurons. Tectal injections led to prominent labeling along the horizontal streak region, with horizontally elongated isodensity contours in both Tyto and Speotyto; retinotectal ganglion cells were heterogeneous and included a group of very large neurons and another group of small neurons, neither of which was labeled from the thalamus. In the visual Wulst, labeled neurons were confined to the supragranular layers after both tectal and thalamic injections. Corticotectal neurons were found in both ipsilateral and contralateral visual Wulst. They were characterized by large cell bodies and prominent dendrites. Corticotectal neurons were distributed throughout the mediolateal extent of the ipsilateral Wulst and therefore involved both the monocular and binocular representations of the visual field. Corticothalamic neurons, found only in the ipsilateral Wulst, were characterized by smaller cell bodies and fine dendrites. They were confined to the monocular crescent on the extreme medial edge of the Wulst.     

A pathway for predation in the brain of the barn owl (Tyto alba): projections of the gracile nucleus to the "claw area" of the rostral wulst via the dorsal thalamus

The Wulst of birds, which is generally considered homologous with the isocortex of mammals, is an elevation on the dorsum of the telencephalon that is particularly prominent in predatory species, especially those with large, frontally placed eyes, such as owls. The Wulst, therefore, is largely visual, but a relatively small rostral portion is somatosensory in nature. In barn owls, this rostral somatosensory part of the Wulst forms a unique physical protuberance dedicated to the representation of the contralateral claw. Here we investigate whether the input to this "claw area" arises from dorsal thalamic neurons that, in turn, receive their somatosensory input from the gracile nucleus. After injections of biotinylated dextran amine into the gracile nucleus and cholera toxin B chain into the claw area, terminations from the former and retrogradely labeled neurons from the latter overlapped substantially in the thalamic nucleus dorsalis intermedius ventralis anterior. These results indicate the existence in this species of a "classical" trisynaptic somatosensory pathway from the body periphery to the telencephalic Wulst, via the dorsal thalamus, one that is likely involved in the barn owl's predatory behavior. The results are discussed in the context of somatosensory projections, primarily in this and other avian species.     

Projections of nucleus angularis and nucleus laminaris to the lateral lemniscal nuclear complex of the barn owl

Interaural phase and intensity are cues by which the barn owl determines, respectively, the azimuth and elevation of a sound source. Physiological studies indicate that phase and intensity are processed independently in the auditory brainstem of the barn owl. The phases of spectral components of a sound are encoded in nucleus magnocellularis (NM), one of the two cochlear nuclei. NM projects solely and bilaterally to nucleus laminaris (NL), wherein interaural phase difference is computed. The other cochlear nucleus, nucleus angularis (NA), encodes the amplitudes of spectral components of sounds. We report here the projections of NA and NL to the lateral lemniscal nuclei of the barn owl. The lateral lemniscal complex comprises nucleus olivaris superior (SO); nucleus lemnisci lateralis, pars ventralis (LLv); and nucleus ventralis lemnisci lateralis (VLV). At caudal levels, VLV may be divided into a posterior (VLVp) and an anterior (VLVa) subdivision on cytoarchitectonic grounds. At rostral levels, the cytoarchitectural differences diminish and the boundaries between the two subdivisions become obscured. Likewise, our data from anterograde tracing studies suggest that at caudal levels the terminal fields of NA and NL remain confined to VLVp and VLVa, respectively. They merge, however, at rostral levels. The data also suggest that NL projects to the medial portion of the ipsilateral SO and that NA projects bilaterally to all parts of SO and LLv. Studies with the retrograde transport of horseradish peroxidase confirm these projections.     

Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl

The cochlear nucleus of the barn owl is composed of two anatomically distinct subnuclei, n. magnocellularis (the magnocellular nucleus) and n. angularis (the angular nucleus). In the magnocellular nucleus, neurons tend to respond at a particular phase of a stimulus sine wave. Phase locking was observed for frequencies up to 9.0 kHz. The intensity-spike count functions of magnocellular units are characterized by high rates of spontaneous activity, a narrow range of intensities over which spike counts changed from spontaneous to saturation levels, and a small increase in spike counts with intensity over that range. In the angular nucleus, neurons showed little or no tendency to respond at a certain sinusoidal phase, although some showed weak phase locking for frequencies below 3.5 kHz. Angular units typically had low spontaneous rates, large dynamic ranges, and large increases in spike counts with intensity, resulting in high saturation levels. The clear difference between the two nuclei in sensitivity to both phase and intensity and the reciprocity in response properties support the hypothesis that each nucleus is specialized to process one parameter (phase or intensity) and not the other.     

Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl

The barn owl determines the directions from which sounds emanate by computing the interaural differences in the timing and intensity of sounds. These cues for sound localization are processed in independent channels originating at nucleus magnocellularis (NM) and nucleus angularis (NA), the cochlear nuclei. The cells of NM are specialized for encoding the phase of sounds in the ipsilateral ear. The cells of NA are specialized for encoding the intensity of sounds in the ipsilateral ear. NM projects solely, bilaterally, and tonotopically to nucleus laminaris (NL). NL and NA project to largely nonoverlapping zones in the central nucleus of the inferior colliculus (ICc), thus forming hodological subdivisions in which time and intensity information may be processed. The terminal field of NL occupies a discrete zone in the rostromedial portion of the contralateral ICc, which we have termed the "core" of ICc. The terminal field of NA surrounds the core of ICc and thus forms a "shell" around it. The projection from NL to the core conserves tonotopy. Low-frequency regions of NL project to the dorsal portions of the core whereas higher-frequency regions project to more ventral portions. This innervation pattern is consistent with earlier physiological studies of tonotopy. Physiological studies have also suggested that NL and the core of ICs contain a representation of the location of a sound source along the horizontal axis. Our data suggest that the projection from NL to the core preserves spatiotopy. Thus, the dorsal portion of NL on the left, which contains a representation of eccentric loci in the right hemifield, innervates the area of the right ICc core that represents eccentric right loci. The more ventral portion of the left NL, which represents loci close to the vertical meridian, innervates the more rostral portions of the right core, which also represents loci near the vertical meridian.     

Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl

Nucleus laminaris (NL) is the site at which the timing of sounds arriving in the 2 ears is compared in the auditory system of the barn owl. Earlier studies have reported vitamin D-dependent calcium binding protein (CaBP)-like immunoreactivity in the somata of NL. We report here that CaBP-like immunoreactivity stains the terminal field of NL. The specific CaBP immunoreactivity is localized to a dense plexus of fibers that have bouton-like swellings, usually around unstained somata. This type of immunoreactivity is found in a restricted portion of the central nucleus of the inferior colliculus (ICc), in the anterior division of the ventral lateral lemniscal complex (VLVA), and in the superior olivary nucleus (SO), all of which have been shown by anterograde transport of 3H-proline to be innervated by NL. The immunoreactivity is absent from the posterior division of ventral lateral lemniscal complex and from the region that surrounds the portion of ICc innervated by NL. A restricted lesion in NL results in a localized deficit in immunoreactivity in those regions of ICc and VLVA that are known to be innervated by the lesioned area of NL. In adjacent sections processed by the Fink-Heimer method, degenerating axons are present in the region of the deficit in immunoreactivity.     

Early visual experience shapes the representation of auditory space in the forebrain gaze fields of the barn owl.

Auditory spatial information is processed in parallel forebrain and midbrain pathways. Sensory experience early in life has been shown to exert a powerful influence on the representation of auditory space in the midbrain space-processing pathway. The goal of this study was to determine whether early experience also shapes the representation of auditory space in the forebrain. Owls were raised wearing prismatic spectacles that shifted the visual field in the horizontal plane. This manipulation altered the relationship between interaural time differences (ITDs), the principal cue used for azimuthal localization, and locations of auditory stimuli in the visual field. Extracellular recordings were used to characterize ITD tuning in the auditory archistriatum (AAr), a subdivision of the forebrain gaze fields, in normal and prism-reared owls. Prism rearing altered the representation of ITD in the AAr. In prism-reared owls, unit tuning for ITD was shifted in the adaptive direction, according to the direction of the optical displacement imposed by the spectacles. Changes in ITD tuning involved the acquisition of unit responses to adaptive ITD values and, to a lesser extent, the elimination of responses to nonadaptive (previously normal) ITD values. Shifts in ITD tuning in the AAr were similar to shifts in ITD tuning observed in the optic tectum of the same owls. This experience-based adjustment of binaural tuning in the AAr helps to maintain mutual registry between the forebrain and midbrain representations of auditory space and may help to ensure consistent behavioral responses to auditory stimuli.     

Response properties of neurons in the core of the central nucleus of the inferior colliculus of the barn owl

The central nucleus of the inferior colliculus (ICC) is particularly important for the processing of interaural time differences (ITDs). In the barn owl, neuronal best frequencies in a subnucleus of the ICC, the ICCcore, span the animal's entire hearing range (approximately equal to 200-10 000 Hz). This means that low-frequency ITD-sensitive ICCcore neurons in the owl can be directly compared to ITD-sensitive mammalian ICC neurons with similar best frequencies as well as to the high-frequency ITD-sensitive neurons usually studied in owls. This report represents a first attempt to systematically describe important physiological properties of ICCcore neurons in the barn owl, with particular attention to the low-frequency region (< 2 kHz). Responses were obtained from 133 neurons or small clusters of neurons; recording sites were confirmed by histological reconstruction of electrode tracks based on electrolytic lesions. Iso-intensity frequency response functions were typically approximately equal to 1 octave wide in the low-frequency range and approximately equal to 1/3 octave wide in the high-frequency range. Most neurons were ITD-tuned; both noise and pure tone stimuli yielded periodic ITD tuning curves with several equivalent response maxima. In most cases ITD tuning curves had a response peak within the barn owl's physiological ITD range. ITD tuning widths were inversely correlated with neuronal best frequency. None of the ICCcore neurons studied were sensitive to interaural level differences. Monaural inputs to ICCcore cells were typically binaurally balanced, i.e. they exhibited similar response thresholds, dynamic ranges, slopes and saturation levels, for both left and right ear monaural stimulation.     

Central projections of auditory nerve fibers in the barn owl.

The central projections of the auditory nerve were examined in the barn owl. Each auditory nerve fiber enters the brain and divides to terminate in both the cochlear nucleus angularis and the cochlear nucleus magnocellularis. This division parallels a functional division into intensity and time coding in the auditory system. The lateral branch of the auditory nerve innervates the nucleus angularis and gives rise to a major and a minor terminal field. The terminals range in size and shape from small boutons to large irregular boutons with thorn-like appendages. The medial branch of the auditory nerve conveys phase information to the cells of the nucleus magnocellularis via large axosomatic endings or end bulbs of Held. Each medial branch divides to form 3-6 end bulbs along the rostrocaudal orientation of a single tonotopic band, and each magnocellular neuron receives 1-4 end bulbs. The end bulb envelops the postsynaptic cell body and forms large numbers of synapses. The auditory nerve profiles contain round clear vesicles and form punctate asymmetric synapses on both somatic spines and the cell body.     

Acetylcholinesterase staining differentiates functionally distinct auditory pathways in the barn owl

The aim of this study was to examine how the functional specialization of the barn owl's auditory brainstem might correlate with histochemical compartmentalizaiton. The barn owl uses interaural intensity and time differences to encode, respectively, the vertical and azimuthal positions of sound sources in space. These two auditory cues are processed in parallel ascending pathways that separate from each other at the level of the cochlear nuclei. Sections through the auditory brainstem were stained for acetylcholinesterase (AChE) to examine whether nuclei that process different auditory cues stain differentially for this enzyme. Of the two cochlear nuclei, angularis showed more intense staining than nucleus magnocellularis. Nucleus angularis projects to all of the nuclei and subdivisions of nuclei that belong to the intensity processing pathway. Acetylcholinesterase stained all regions that contain terminal fields of nucleus angularis and thus provided discrimination between the time and intensity pathways. Moreover, staining patterns with acetylcholinesterase were complementary to those prevously reported with an anti-calbindin antibody, which stains terminal fields of nucleus laminaris, and thus stains all the nuclei and subdivisions of nuclei that belong to the time pathway. Some of the gross staining patterns observed with AChE were similar to those reported with antibodies to glutamate decarboxylase. However, AChE is a more convenient and definitive marker in discriminating between these pathways than is calbindin or glutamate decarboxylase. Acetylcholinesterase staining of the intensity pathway in the owl may be related to encoding of sound intensity by spike rate over large dynamic ranges. © 1993 Wiley-Liss, Inc.     

Distribution of GABAergic neurons and terminals in the auditory system of the barn owl

Antisera to GAD (glutamic acid decarboxylase) and GABA were used to determine the distribution of GABAergic cells and terminals in the brainstem and midbrain auditory nuclei of the barn owl. The owl processes time and intensity components of the auditory signal in separate pathways, and each pathway has a distinctive pattern of GAD- and GABA-like immunoreactivity. In the time pathway, all the cells of the cochlear nucleus magnocellularis and nucleus laminaris receive perisomatic GABAergic terminals, and small numbers of GABAergic neurons surround both nuclei. The ventral nucleus of the lateral lemniscus (anterior division) contains both immunoreactive terminals and some GABAergic neurons. In the intensity pathway, dense immunoreactive terminals are distributed throughout the cochlear nucleus angularis, which also contains a small number of GABAergic neurons. The superior olive contains two GABAergic cell types and immunoreactive terminals distributed throughout the neuropil. All the neurons of the nucleus of the lateral lemniscus (ventral part) appear to be GABAergic, and this nucleus also contains a moderate number of immunoreactive terminals. Immunoreactive terminals are distributed throughout the neuropil of the ventral nucleus of the lateral lemniscus (posterior division), whereas multipolar and small fusiform GABAergic neurons predominate in the dorsal regions of the nucleus. The time and intensity pathways combine in the inferior colliculus. The central nucleus of the inferior colliculus contains a larger number of fusiform and stellate GABAergic neurons and a dense plexus of immunoreactive terminals, whereas the external nucleus contains slightly fewer immunoreactive cells and terminals. The superficial nucleus contains dense, fine immunoreactive terminals and a small number of GABAergic neurons.     

Localization of AMPA-selective glutamate receptors in the auditory brainstem of the barn owl

AMPA receptor subunit-specific antibodies were used to determine if the distribution of excitatory amino acid receptors in the owl's auditory brainstem and midbrain nuclei reflected specializations for temporal processing. Each auditory nucleus displays characteristic levels of immunostaining for the AMPA receptor subunits GluR1–4, with high levels of the subtypes which exhibit rapid desensitization (GluR4 and 2/3). In the auditory brainstem, levels of GluR2/3 and GluR4 were very high in the cochlear nucleus magnocellularis and the nucleus laminaris. The different cell types of the cochlear nucleus angularis and the superior olive were characterized by heterogeneous GluR2/3 and 4 immunostaining. GluR1 levels were very low or undetectable. In the lemniscal nuclei, most neurons contained low levels of GluR1, and dense GluR2/3 and GluR4 immunoreactivity, with high levels of GluR4 in the dendrites. Levels of GluR4 were higher in the anterior portion of the ventral nucleus of the lateral lemniscus. The divisions of the inferior colliculus could be distinguished on the basis of GluR1–4 immunoreactivity, with high levels of GluR4 and moderate levels of GluR1 in the external nucleus. No major differences were observed between the pathways for encoding time and sound level cues. J. Comp. Neurol. 378:239–253, 1997. © 1997 Wiley-Liss, Inc.     

Abnormalities of the nucleus basalis in Down's syndrome

One of the most striking manifestations of Down's syndrome is profound mental retardation. Furthermore, after 35 years of age, many patients with Down's syndrome develop clinical and pathological features of Alzheimer's disease. Since brains of patients with Alzheimer's disease show significant loss of neurons in the nucleus basalis of Meynert (nbM), we sought to establish normal standards of nbM neurons in persons with Down's syndrome and to determine whether reductions in the number of neurons occur with increasing age. The number and size of neurons in the nbM were measured in selected sagittal sections from 5 patients with Down's syndrome and 5 age-matched controls. The patients (age range, 16 to 56 years) had 29% fewer nbM neurons than controls, and the oldest patient had the lowest cell count of all subjects. The size of nbM neurons did not differ significantly between the two groups. Our results show that the nbM contains fewer neurons in young persons with Down's syndrome than in normal controls and suggest that the number of these nerve cells may be further reduced in older persons with Down's syndrome.