Development of the projection from the nucleus of the brachium of the inferior colliculus to the superior colliculus in the ferret (original) (raw)
Related papers
Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex
Nature Neuroscience, 2003
Auditory localization relies on the detection and interpretation of acoustic cues that change in value as the head and external ears grow. Here we show that the maturation of these structures is an important determinant for the development of spatial selectivity in the ferret auditory cortex. Spatial response fields (SRFs) of high-frequency cortical neurons recorded at postnatal days (P) 33-39 were broader, and transmitted less information about stimulus direction, than in older ferrets. They also exhibited slightly broader frequency tuning than neurons recorded in adult animals. However, when infant neurons were stimulated through virtual ears of adults, SRFs sharpened significantly and the amount of transmitted information increased. This improvement was predicted by a model that generates SRF shape from the localization cue values and the neurons' binaural spectrotemporal response properties. The maturation of spatial response characteristics in auditory cortex therefore seems to be limited by peripheral rather than by central factors.
Eur J Neurosci, 2000
The normal maturation of the auditory space map in the deeper layers of the ferret superior colliculus (SC) depends on signals provided by the super®cial visual layers, but it is unknown where or how these signals in¯uence the developing auditory responses. Here we report that tracer injections in the super®cial layers label axons with en passant and terminal boutons, both in the deeper layers of the SC and in their primary source of auditory input, the nucleus of the brachium of the inferior colliculus (nBIC). Electron microscopy con®rmed that biocytin-labelled SC axons form axodendritic synapses on nBIC neurons. Injections of biotinylated dextran amine in the nBIC resulted in anterograde labelling in the deeper layers of the SC, as well as retrogradely labelled super®cial and deep SC neurons, whose distribution varied systematically with the rostrocaudal placement of the injection sites in the nBIC. Topographical order in the projection from the SC to the ipsilateral nBIC was con®rmed usinḡ uorescent microspheres. We demonstrated the existence of functional SC-nBIC connections by making whole-cell current-clamp recordings from young ferret slices. Both monosynaptic and polysynaptic EPSPs were generated by electrical stimulation of either the super®cial or deep SC layers. In addition to unimodal auditory units, both visual and bimodal visual±auditory units were recorded in the nBIC in vivo and their incidence was higher in juvenile ferrets than in adults. The SC-nBIC circuit provides a potential means by which visual and other sensory or premotor signals may be delivered to the nBIC to calibrate the representation of auditory space.
The Journal of Neuroscience, 1998
We have examined whether the superficial layers of the superior colliculus (SC) provide the source of visual signals that guide the development of the auditory space map in the deeper layers. Anatomical tracing experiments with fluorescent microspheres revealed that a retinotopic map is present in the newborn ferret SC. Aspiration of the caudal region of the superficial layers of the right SC on postnatal day 0 did not cause a reorganization of this projection. Consequently, recordings made when the animals were mature showed that visual units in the remaining superficial layers in rostral SC had receptive fields that spanned a restricted region of anterior space. Auditory units recorded beneath the remaining superficial layers were tuned to corresponding anterior locations. Both the superficial layer visual map and the deeper layer auditory map were normal in the left, unoperated SC. The majority of auditory units recorded throughout the deeper layers ventral to the superficial lay...
European Journal of Neuroscience, 1990
ABSTRACT Guinea pigs, reared from birth in an environment of omnidirectional white noise, fail to develop a map of auditory space in the deeper layers of the superior colliculus. Collicular responses from such noise-reared animals reveal large auditory spatial receptive fields. The representation of auditory space in the colliculus shows no topographic order. Exposing developing animals to the noise environment only for restricted time periods showed that animals reared normally up to 26 days after birth (DAB) and then placed in the noise chamber could not construct spatial maps, whereas animals reared normally to 30 DAB and then placed in the noise chamber until the terminal mapping experiment could construct topographically organized spatial maps with local receptive fields. Limiting the noise exposure to the period between 26 and 30 DAB was sufficient to prevent spatial map formation. The failure to form a map of auditory space did not reflect environmental damage to the cochlea or the functional organization of the primary auditory pathway. The response thresholds of cochlear microphonics and of auditory responses in both the inferior and superior colliculus were normal in noise-reared animals. Similarly normal were the tonotopic organization and frequency tuning characteristics of inferior collicular neurons. The rearing environment thus appears to exert a selective effect upon the maturation of the superior collicular map of auditory space. We attribute this effect to the masking, by the omnidirectional broad-band noise, of discrete localized auditory stimuli. Cues deriving from these latter stimuli would appear to be necessary for the elaboration of the map of auditory space. This auditory experience operates during a 4 day crucial developmental period from 26 to 30 DAB. This is the same developmental time window as that during which visual experience is required for the construction of the map.
Journal of neurophysiology, 1998
Spectral localization cues provided by the outer ear are utilized in the construction of the auditory space map in the superior colliculus (SC). The role of the outer ear in the development of this map was examined by recording from the SC of anesthetized, adult ferrets in which the pinna and concha had been removed in infancy. The acoustical consequences of this procedure were assessed by recording outer ear impulse responses via a probe-tube microphone implanted in the wall of the ear canal. Both monaural and binaural spectral cues normally show a number of asymmetric features within the horizontal plane, which allow azimuthal locations on either side of the interaural axis to be discriminated. These features were eliminated or altered by chronic pinnectomy. The responses of auditory units in the SC to noise bursts presented in the free field were examined at sound levels of approximately 10 and 25 dB above unit threshold. After bilateral pinnectomy, the representation of auditory...
Development, Organization and Plasticity of Auditory Circuits: Lessons from a Cherished Colleague
The European journal of neuroscience, 2018
Ray Guillery was a neuroscientist known primarily for his ground-breaking studies on the development of the visual pathways and subsequently on the nature of thalamocortical processing loops. The legacy of his work, however, extends well beyond the visual system. Thanks to Ray Guillery's pioneering anatomical studies, the ferret has become a widely used animal model for investigating the development and plasticity of sensory processing. This includes our own work on the auditory system, where experiments in ferrets have revealed the role of sensory experience during development in shaping the neural circuits responsible for sound localization, as well as the capacity of the mature brain to adapt to changes in inputs resulting from hearing loss. Our research has also built on Ray Guillery's ideas about the possible functions of the massive descending projections that link sensory areas of the cerebral cortex to the thalamus and other subcortical targets, by demonstrating a ro...
Plasticity in the neural coding of auditory space in the mammalian brain
Proceedings of the National Academy of Sciences, 2000
Sound localization relies on the neural processing of monaural and binaural spatial cues that arise from the way sounds interact with the head and external ears. Neurophysiological studies of animals raised with abnormal sensory inputs show that the map of auditory space in the superior colliculus is shaped during development by both auditory and visual experience. An example of this plasticity is provided by monaural occlusion during infancy, which leads to compensatory changes in auditory spatial tuning that tend to preserve the alignment between the neural representations of visual and auditory space. Adaptive changes also take place in sound localization behavior, as demonstrated by the fact that ferrets raised and tested with one ear plugged learn to localize as accurately as control animals. In both cases, these adjustments may involve greater use of monaural spectral cues provided by the other ear. Although plasticity in the auditory space map seems to be restricted to development, adult ferrets show some recovery of sound localization behavior after long-term monaural occlusion. The capacity for behavioral adaptation is, however, task dependent, because auditory spatial acuity and binaural unmasking (a measure of the spatial contribution to the "cocktail party effect") are permanently impaired by chronically plugging one ear, both in infancy but especially in adulthood. Experience-induced plasticity allows the neural circuitry underlying sound localization to be customized to individual characteristics, such as the size and shape of the head and ears, and to compensate for natural conductive hearing losses, including those associated with middle ear disease in infancy.
1995 Feliciano et al AN Direct projections from the rat primary auditory neocortex
It has generally been accepted that neocortical projections to the auditory brainstem do not extend beyond the level of the inferior colliculus. Consequently, it has been assumed that the neocortical influence on lower auditory nuclei is necessarily conveyed by the inferior colliculus. Nevertheless, severa} isolated reports suggest that ablation of the auditory neocortex results in degenerating fibers in the lateral lemniscus, superior olivary complex, and cochlear nuclei, thus challenging the previous tenet. In an attempt to verify the existence of direct neocortical projections to subcollicular auditory nudei and to determine the trajectories, topography, morphology, and possible targets of presumptive corticopontobulbar projections, the anterograde axonal tracers Phaseolus vulgaris-leukoagglutinin and biotinylated dextran were iontophoretically injected at different locations within the primary auditory neocortex of adult albino rats. Terminal anterograde labeling was consistently found: (1) ipsilaterally, in regions surrounding the nudei of the lateral lemniscus, including the nucleus sagulum, the horizontal cell group region (which separates dorsal and intennediate nuclei of the lateral lemniscus), and the rostral and medial paralemniscal regions; (2) bilaterally, in different subdivisions of the superior olivary complex, notably the ventral nucleus of the trapezoid body and the lateral superior olive, as well as a narrow and ill-defined region that overlies the dorsal aspect of the superior olivary complex; and bilaterally, in the dorsal cochlear •Corresponding author: Dr. Enrico Mugnaini, Lab. of Neuromorphology, Biobehavioral Science Graduate Degree Program, University of Connecticut, Box U-154, 3107 Horse Bam Hill Road, Storrs, CT nudeus and in the subregions of the granule cell domain that surround the ventral cochlear nudeus. The neocortical fibers directed to these subcollicular auditory centers travel in the ipsilateral cerebral pedunde, which they leave at different mesencephalic and rhombencephalic levels to follow specific routes to their targets. The nuclei of the lateral lemniscus themselves, the major nuclei of the superior olivary complex (with the exception of the lateral superior olive), and the magnocellular regions of the ventral cochlear nucleus were devoid of terminal labeling. The auditory corticosubcollicularprojections seem to innervate peripheral cell groups of the auditory pathway whose roles in sound processing have not been firmly established, but they do not seem to target the major nuclei of the lower auditory brainstem, which have more clearly defined roles in hearing. otinylated d extran THE AUDITORY CEREBRAL cortex is the final target of the ascending auditory pathways of the mammalian brain and plays a key role in the integration and processing of cognitive and affective aspects of acoustic information. The auditory neocortex is also the starting point for intrinsic, callosa! and descending (or corticofugal) projections. Although the corticofugal fibers innerva te nonauditory neural centers, including the cauda te putamen, the superior colliculus, and the pontine nuclei, their main targets are auditory diencephalic and mesencephalic structures, notably the medial geniculate body and the inferior colliculus (IC) (Andersen et al., 1980a, b;. Although medial geniculate 287
Experimental Brain Research, 1993
There have been conflicting reports concerning the importance of visual experience in the development of auditory localization mechanisms. We have examined the representation of auditory space in the superior colliculus of adult ferrets that were visually deprived by binocular eyelid suture from postnatal days 25-28, prior to natural eye opening, until the time of recording. This procedure attenuated the transmission of light by a factor of at least 20-25 and blurred the image so that, as long as the eyelids were still fused, the responses of visual units in the superficial layers of the superior colliculus were labile and very poorly tuned. After the eyelids were opened, the representation of the visual field in these layers appeared to be normal. Acoustically responsive units were, as usual, almost exclusively restricted to the deeper layers of the superior colliculus. However, unlike normal animals, where responses occurring only at stimulus onset predominate, most of these units exhibited sustained or multi-peaked discharge patterns. The degree of spatial tuning of individual units recorded from the normal and deprived groups of animals was not significantly different in either azimuth or elevation. Normally orientated maps of both sound azimuth and elevation were also found in the visually deprived ferrets. However, abnormalities were present in the topography and precision of these representations and consequently in their alignment with the overlying visual map. In particular, an increase was observed in the proportion of auditory units with spatially ambiguous receptive fields, in which the maximum response occurred at two distinct locations. These results indicate that patterned visual experience is not required for establishing at least a crude map of auditory space in the superior colliculus, but suggest that it may play a role in refining this representation during development.
Coding for auditory space in the superior colliculus of the rat
European Journal of Neuroscience, 2000
Although the rat is often used to determine behavioural sound-localization capabilities or neuronal computation of binaural information, the representation of auditory space in the rat brain has not been investigated so far. We obtained extracellular recordings from auditory neurons in the superior colliculus of anaesthetized rats and examined them for spatial tuning characteristics and topographical order. Many neurons (73%) showed significant tuning, with a single peak in the azimuth response profiles based on spike rates and response latencies. Best azimuth values from neurons in one SC were generally tuned to contralateral and rarely to frontal or ipsilateral directions. Tuning width was mostly broad; at supra-threshold sound pressure levels (35 dB SPL), 55% of the units had a tuning width of > 120 degrees in contralateral space. Additionally, tuning width increased with stimulation intensity. A significant but considerably scattered topographical order of best azimuth directions was observed in the deep layers of the superior colliculus with frontal directions being represented closer to the rostral pole. Tuned auditory units in the intermediate layers of the superior colliculus, however, showed no systematic spatial arrangement. This pattern was confirmed by analysing best azimuth directions from simultaneously recorded units. Our results indicate that the rat superior colliculus contains a representation of auditory space which is similar to that described for other small mammals.