Development, Organization and Plasticity of Auditory Circuits: Lessons from a Cherished Colleague (original) (raw)
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The Ferret Auditory Cortex: Descending Projections to the Inferior Colliculus
Cerebral Cortex, 2006
Descending corticofugal projections are thought to play a critical role in shaping the responses of subcortical neurons. Here, we examine the origins and targets of ferret auditory corticocollicular projections. We show that the ectosylvian gyrus (EG), where the auditory cortex is located, can be subdivided into middle, anterior, and posterior regions according to the pattern of cytochrome oxidase staining and immunoreactivity for the neurofilament antibody SMI 32 . Injection of retrograde tracers in the inferior colliculus (IC) labeled large layer V pyramidal cells throughout the EG and adjacent sulci. Each region of the EG has a different pattern of descending projections. Neurons in the primary auditory fields in the middle EG project to the lateral nucleus (LN) of the ipsilateral IC and bilaterally to the dorsal cortex and dorsal part of the central nucleus (CN). The projection to these dorsomedial regions of the IC is predominantly ipsilateral and topographically organized. The secondary cortical fields in the posterior EG target the same midbrain areas but exclude the CN of the IC. A smaller projection to the ipsilateral LN also arises from the anterior EG, which is the only region of auditory cortex to target tegmental areas surrounding the IC, including the superior colliculus, periaqueductal gray, intercollicular tegmentum, and cuneiform nucleus. This pattern of corticocollicular connectivity is consistent with regional differences in physiological properties and provides another basis for subdividing ferret auditory cortex into functionally distinct areas.
The Journal of Comparative Neurology, 1990
The organization of cortical circuitry responsible for processing sensory information is a subject of intense examination. However, it is not known whether cortical cells in different sensory cortices process information in a way that is specific to the modality of their input, or whether there are commonalities in processing circuitry across different cortices. In our laboratory, this question has been investigated at the level of the geniculocortical pathway by routing information of one sensory modality into the processing circuitry of another modality. Appropriate early lesions cause growth of retinal axons into the auditory thalamus (MGN) (Sur et al., Science 2421437, '88). Previously, we have established that the MGN carries the resulting visual information on to primary auditory cortex (AI), which thus contains visually responsive neurons and a topographic representation of the retina (Roe et al., SOC. Neurosci. Abstr. 14:460, '88; Sur et al., Science 2421437, '88). In this paper, we describe anomalous projections from the dorsal part of the thalamus, specifically the lateral posterior/pulvinar complex, into AI. This result demonstrates that thalamic neurons belonging to one modality can be induced to project to cortex that is normally of a different modality. In addition, we have studied in detail the nature of the MGN to AI projection in these animals as compared to the normal projection. The MGN to AT projection appears to be unaltered by the lesions; the location and topography of labelled cells are similar to that in normal animals. Because the MGN to AI projection is still highly divergent along the "isofrequency" dimension when compared to the tonotopic dimension, our data suggest that visual topography in the cortical map is created within the auditory cortex, perhaps by activity-dependent sharpening of the retinal representation during development.
The Journal of Neuroscience, 1992
ulate nucleus, or MGN). Retinal afferents subsequently provide visual input to cells in primary auditory cortex (Al) of the "rewired" ferret (Sur et al., 1988) and establish a topographic visual map there (Roe et al., 1990a). We have now examined both qualitatively and quantitatively the physiological response properties of single visual units in Al of rewired ferrets and compared them to the properties ofcells in primary visual cortex (V 1) of normal ferrets. A preliminary report of these data has been published previously (Roe et al., 1990b).
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...
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.
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 Comparative Neurology, 1993
We have previously reported that following specific neonatal brain lesions in ferrets, a retinal projection is induced into the auditory thalamus (Sur et al., Science 242:1437, '88). In these "rewired" ferrets, a novel visual pathway is established through auditory thalamus [the medial geniculate nucleus (MGN)] and primary auditory cortex (All; cells in both MGN and A1 are visually responsive and exhibit properties similar to those of visual cells in the normal visual pathway. In this paper, we use three approaches-physiological, anatomical, and developmental-to examine which of the retinal ganglion cells project to the MGN in these rewired ferrets. We find that: 1) physiological response properties of postsynaptic visual cells in the MGN are W-like; 2) retinal ganglion cells back-filled from the MGN are small and similar to soma sizes of subsets of the normal retinal W cell population; and 3) subpopulations of these small cells can be preferentially rerouted to the MGN in response to different surgical manipulations at birth, consistent with differential W cell projection patterns in normal animals. These data suggest that retinal W cells come to project to the MGN in rewired animals. These findings not only provide a basis on which to interpret functional properties of this novel visual pathway, but also provide important information about the developmental capabilities of specific retinal ganglion cell classes and the regulation of their projections by target structures in the brain during development.
Functional organization of ferret auditory cortex
2005
We characterized the functional organization of different fields within the auditory cortex of anaesthetized ferrets. As previously reported, the primary auditory cortex, A1, and the anterior auditory field, AAF, are located on the middle ectosylvian gyrus. These areas exhibited a similar tonotopic organization, with high frequencies represented at the dorsal tip of the gyrus and low frequencies more ventrally, but differed in that AAF neurons had shorter response latencies than those in A1. On the basis of differences in frequency selectivity, temporal response properties and thresholds, we identified four more, previously undescribed fields. Two of these are located on the posterior ectosylvian gyrus and were tonotopically organized. Neurons in these areas responded robustly to tones, but had longer latencies, more sustained responses and a higher incidence of non-monotonic rate-level functions than those in the primary fields. Two further auditory fields, which were not tonotopically organized, were found on the anterior ectosylvian gyrus. Neurons in the more dorsal anterior area gave short-latency, transient responses to tones and were generally broadly tuned with a preference for high (>8 kHz) frequencies. Neurons in the other anterior area were frequently unresponsive to tones, but often responded vigorously to broadband noise. The presence of both tonotopic and non-tonotopic auditory cortical fields indicates that the organization of ferret auditory cortex is comparable to that seen in other mammals.
Visual influences on ferret auditory cortex
Hearing Research, 2009
Multisensory neurons are now known to be widespread in low-level regions of the cortex usually thought of as being responsible for modality-specific processing. The auditory cortex provides a particularly striking example of this, exhibiting responses to both visual and somatosensory stimulation. Single-neuron recording studies in ferrets have shown that each of auditory fields that have been characterized using physiological and anatomical criteria also receives visual inputs, with the incidence of visually-sensitive neurons ranging from 15% to 20% in the primary areas to around 50% or more in higher-level areas. Although some neurons exhibit spiking responses to visual stimulation, these inputs often have subthreshold influences that modulate the responses of the cortical neurons to sound. Insights into the possible role played by the visual inputs can be obtained by examining their sources of origin and the way in which they alter the processing capabilities of neurons in the auditory cortex. These studies suggest that one of the functions of the visual input to auditory cortex is to sharpen the relatively imprecise spatial coding typically found there. Because the extent to which this happens varies between cortical fields, the investigation of multisensory interactions can also help in understanding their relative contributions to auditory perception.
Lesions of the Auditory Cortex Impair Azimuthal Sound Localization and Its Recalibration in Ferrets
Journal of Neurophysiology, 2010
[PDF] [Full Text] [Abstract] , January , 2013; 136 (1): 180-193. Brain Single-sided deafness leads to unilateral aural preference within an early sensitive period [PDF] [Full Text] [Abstract] , April 10, 2013; 33 (15): 6659-6671. [PDF] [Full Text] [Abstract] , June 5, 2013; 33 (23): 9693-9698. Nodal FR, Kacelnik O, Bajo VM, Bizley JK, Moore DR, King AJ.