Ferret Superior Colliculus Research Articles

Layer dependent visual receptive field properties in ferret superior colliculus

Event Abstract Back to Event Layer dependent visual receptive field properties in ferret superior colliculus Iain Stitt1*, Edgar Galindo-Leon1, Florian Pieper1, Gerhard Engler1 and Andreas Engel1 1 Institute for Neurophysiology and Pathophysiology, Universitätsklinikum Hamburg-Eppendorf, Germany The mammalian superior colliculus (SC) is a highly conserved midbrain structure that responds to novel external events and initiates orienting movements. Interestingly, all layers of the SC, regardless of modality, are organised into juxtaposed, overlaid maps of space. Recent anatomical studies have provided evidence for a direct superficial-to-deep projection in the SC. However, it remains unclear how much information is conveyed by this connectivity. Here, we recorded single and multi-unit activity, along with local field potentials from both superficial and deep layers of the SC with a dual-shank silicon multichannel probe. Spatial receptive fields of the neurons were determined using small (~3°) drifting gratings presented at 20x20 different locations on a rear projection screen. The location of spatial receptive fields recorded within individual SC penetrations were very similar, as predicted by anatomical connectivity. To assess directional/orientation tuning characteristics across SC layers, full field drifting gratings were presented with 8 directions spaced equally over 360 degrees. Of visually responsive units, 22% were classified as orienatation selective, 7% of were classified as direction selective, and 5% units displayed characteristics that were intermediate to both classifications. Correlation in feature selectivity between recording sites was greatest at neighbouring electrodes, and decreased proportionally with distance between recording sites. Previous studies have focused on the visual receptive field properties of neurons in the superficial, retinorecipient layers of the SC. In this study, we record from the entire laminar structure of the SC to assess the physiological relevance of the anatomically defined superficial-to-deep projection. Keywords: Perception, superior colliculus Conference: XI International Conference on Cognitive Neuroscience (ICON XI), Palma, Mallorca, Spain, 25 Sep - 29 Sep, 2011. Presentation Type: Poster Presentation Topic: Poster Sessions: Neurophysiology of Sensation and Perception Citation: Stitt I, Galindo-Leon E, Pieper F, Engler G and Engel A (2011). Layer dependent visual receptive field properties in ferret superior colliculus. Conference Abstract: XI International Conference on Cognitive Neuroscience (ICON XI). doi: 10.3389/conf.fnhum.2011.207.00361 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 23 Nov 2011; Published Online: 28 Nov 2011. * Correspondence: Dr. Iain Stitt, Institute for Neurophysiology and Pathophysiology, Universitätsklinikum Hamburg-Eppendorf, Hamburg, Germany, i.stitt@uke.de Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Iain Stitt Edgar Galindo-Leon Florian Pieper Gerhard Engler Andreas Engel Google Iain Stitt Edgar Galindo-Leon Florian Pieper Gerhard Engler Andreas Engel Google Scholar Iain Stitt Edgar Galindo-Leon Florian Pieper Gerhard Engler Andreas Engel PubMed Iain Stitt Edgar Galindo-Leon Florian Pieper Gerhard Engler Andreas Engel Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Development of the projection from the nucleus of the brachium of the inferior colliculus to the superior colliculus in the ferret

Neurons in the deeper layers of the superior colliculus (SC) have spatially tuned receptive fields that are arranged to form a map of auditory space. The spatial tuning of these neurons emerges gradually in an experience-dependent manner after the onset of hearing, but the relative contributions of peripheral and central factors in this process of maturation are unknown. We have studied the postnatal development of the projection to the ferret SC from the nucleus of the brachium of the inferior colliculus (nBIC), its main source of auditory input, to determine whether the emergence of auditory map topography can be attributed to anatomical rewiring of this projection. The pattern of retrograde labeling produced by injections of fluorescent microspheres in the SC on postnatal day (P) 0 and just after the age of hearing onset (P29), showed that the nBIC-SC projection is topographically organized in the rostrocaudal axis, along which sound azimuth is represented, from birth. Injections of biotinylated dextran amine-fluorescein into the nBIC at different ages (P30, 60, and 90) labeled axons with numerous terminals and en passant boutons throughout the deeper layers of the SC. This labeling covered the entire mediolateral extent of the SC, but, in keeping with the pattern of retrograde labeling following microsphere injections in the SC, was more restricted rostrocaudally. No systematic changes were observed with age. The stability of the nBIC-SC projection over this period suggests that developmental changes in auditory spatial tuning involve other processes, rather than a gross refinement of the projection from the nBIC.

Spatial distribution of functional superficial–deep connections in the adult ferret superior colliculus

Numerous studies have identified connections between the superficial visual and deeper multisensory layers of the superior colliculus (SC), but the functional distribution of the superficial–deep projection has not been mapped. This question was assessed in the present study using extracellular electrophysiological stimulation and recording techniques. In vitro slices from adult ferrets were used to functionally map the rostro-caudal, medio-lateral, and dorso-ventral distribution of these superficial–deep connections. For each coronal ( n=6) or parasagittal ( n=10) slice, single and multi-unit responses to electrical stimulation of a point in the superficial layers were systematically recorded at different locations along a grid (approximately 300 μm intervals) across the slice. Recording sites with similar activation thresholds were grouped on the histological reconstruction of each slice to plot the functional access of superficial stimulation site to the deeper layers. Low intensity stimulation (defined as a current threshold ≤75 μA) activated areas of the subjacent intermediate layers in most cases (75%; 12/16). Higher intensity stimuli (>75–600 μA) accessed larger areas which, in 50% of the slices, extended into the deepest layers of the SC. However, regardless of the rostro-caudal or medio-lateral position of the superficial layer stimulation site, the proportion of the deeper layers activated remained remarkably constant, although the volume of activated deep layer tissue was shifted in each case toward the central regions of the SC. This last observation argues against the precise alignment of the superficial and deep layer visual maps, suggesting instead that the arrangement of the superficial layer projection may more closely relate to the organization of deep layer auditory and/or somatosensory representations.

Chemoarchitecture of GABAergic neurons in the ferret superior colliculus.

gamma-Aminobutyric acid (GABA)ergic neurons are thought to play a key role both in visual processing and in the complex sensory-motor transformations that take place in the mammalian superior colliculus. To understand the organization of GABAergic neurons in the ferret superior colliculus, we applied antisera to several markers of GABAergic function, including GABA, two isoforms of its synthetic enzyme glutamic acid decarboxylase (GAD-65 and GAD-67), and the GABA transporter, GAT-1. We also applied antisera to several calcium binding proteins (calbindin [CB], calretinin [CR], and parvalbumin [PV]) and neuronal nitric oxide synthase (NOS), chemical markers that colocalize with GABA in some areas of the central nervous system. The distribution of GABAergic neurons in the ferret is similar to that of other mammalian species. GABAergic neurons in the ferret superior colliculus were small, morphologically diverse, and widely distributed throughout all layers of the colliculus. As has been shown in other mammalian species, neurons expressing PV, CB, CR, and NOS were differentially distributed in layers and patches throughout the ferret colliculus. None of these markers, however, showed a distribution that mirrored that of GABAergic neurons. Furthermore, few GABAergic neurons colocalized these neurochemical markers. Only 14% of GABAergic neurons in the superficial layers and 18% of neurons in the deeper layers colocalized PV, 14% of GABAergic neurons in the superficial layers and 10% in the deeper layers colocalized CB, and only 1% of GABAergic neurons in both the superficial and deep layers colocalized nitric oxide synthase. Thus, the arrangement of GABAergic neurons in the ferret superior colliculus is broadly distributed and is distinct from other recognized organizational patterns in the superior colliculus.

Representation of sound source direction in the superior colliculus of the guinea pig in a virtual auditory environment.

The deep layers of the superior colliculus (SC) receive visual, auditory, and somatosensory input. A major function of the SC is the control of orientation movements of the eye, head, and pinna. While a topographical map for sound source direction remains elusive in primary auditory structures of mammals, such a map for azimuthal sound source directions has been reported in the deep layers of the SC. Moreover, a gradient of elevation tuning has been also seen in the SC of ferrets and cats. Here we demonstrate that a virtual auditory environment can be used to reveal azimuthal and elevational topography for auditory spatial receptive fields in neurons in the SC of guinea pigs. Individual, head-related transfer functions (HRTF) were measured in ten guinea pigs for 122 directions in the upper hemispheric field and convolved with white noise. Many neurons (39%) in the deep layers showed robust responses to these virtual sounds, and the majority of these neurons had small spatial receptive fields that were restricted to the contralateral hemifield. Best directions varied from 0 degree to 135 degree azimuth along the contralateral side and from --10 degree to 60 degree elevation. Like previous studies using free-field stimulation, a gradient of best azimuth direction was found along the rostral-caudal axis, with rear directions represented caudally and front directions rostrally. The topographical organization for best elevations had not been studied previously in the guinea pig. We found that it roughly followed the mediolateral axis, with preference for high elevations represented medially and low elevations laterally. A similar organization using free-field stimulation has been reported in the ferret.

Topographical projection from the superior colliculus to the nucleus of the brachium of the inferior colliculus in the ferret: convergence of visual and auditory information

The normal maturation of the auditory space map in the deeper layers of the ferret superior colliculus (SC) depends on signals provided by the superficial visual layers, but it is unknown where or how these signals influence the developing auditory responses. Here we report that tracer injections in the superficial 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 confirmed 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 superficial 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 confirmed using fluorescent 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 superficial 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.

Responses to innocuous, but not noxious, somatosensory stimulation by neurons in the ferret superior colliculus

The intermediate and deep layers of the superior colliculus (SC) are known for their role in initiating orienting behaviors. To direct these orienting functions, the SC of some animals (e.g., primates, carnivores) is dominated by inputs from the distance senses (vision, audition). In contrast, the rodent SC relies more heavily on non-visual inputs, such as touch and nociception, possibly as an adaptive response to the proximity of dangers encountered during their somatosensory-dominant search behaviors. The ferret (a carnivore) seems to employ strategies of both groups: above ground they use visual/auditory cues, but during subterranean hunting ferrets must rely on non-visual signals to direct orienting. Therefore, the present experiments sought to determine whether the sensory inputs to the ferret SC reveal adaptations common to functioning in both environments. The results showed that the ferret SC is dominated (63%; 181/286) by visual/auditory inputs (like the cat), rather than by somatosensory inputs (as found in rodents). Furthermore, tactile responses were driven primarily from hair-receptors (like cats), not from the vibrissae (as in rodents). Additionally, while a majority of collicular neurons in rodents respond to brief noxious stimulation, no such neurons were encountered in the ferret SC. A small proportion (4%; 13/286) of the ferret SC neurons were responsive to long-duration (> 5s) noxious stimulation, but further tests could not establish these responses as nociceptive. Collectively, these data indicate that the ferret SC is best adapted for the animal's visual/acoustically guided activities and most closely resembles the SC of its phylogenetic relative, the cat.

Signals from the Superficial Layers of the Superior Colliculus Enable the Development of the Auditory Space Map in the Deeper Layers

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 layer lesion were also tuned to single sound directions. In this region of the SC, however, we observed much greater scatter in the distribution of preferred sound directions and a significant increase in the proportion of units with spatially ambiguous responses. The auditory representation was degraded, although many of these units were also visually responsive. Equivalent lesions of the superficial layers made in adult ferrets did not alter the topographic order in the auditory representation, suggesting that visual activity in these layers may be involved in aligning the different sensory maps in the developing SC.

Intrinsic circuitry of the superior colliculus: pharmacophysiological identification of horizontally oriented inhibitory interneurons.

Much of what is known about the organization of the superior colliculus is based on the arrangement of its external connections. Consequently, there is little information regarding pathways that remain intrinsic to it, even though recent data suggest that a horizontally oriented local circuit may mediate the functional reciprocity among fixation and saccade-related neurons. Therefore, the present experiments sought physiological evidence for neurons intrinsic to the superior colliculus that might participate in a horizontally oriented local circuit. Parasagittal slices of the ferret superior colliculus were prepared for in vitro recording, and 125 intermediate/deep layer neurons were examined in response to electrical stimulation rostral or caudal to the recording site. A substantial proportion (37%) of neurons responded with a prolonged period (means = 59.3 +/- 30 ms) of poststimulus suppression of spontaneous action potential activity. Of the suppressed neurons, most (53%) were disinhibited when the excitatory amino acid receptor antagonists D-2-amino-5-phosphonovaleric acid (D-APV) and 6-nitro-7 sulphamoylbeno[f]-quinoxaline-2,3-dione (NBQX) were administered, indicating that excitatory input to inhibitory interneurons was blocked. Of the neurons that received inputs from inhibitory interneurons, all had their suppressive responses decreased or eliminated by the gamma-aminobutyric acid antagonist, bicuculline. Finally, severing the superficial layers from the slice had no effect on intermediate layer responses to intrinsic stimulation. These data provide physiological evidence for the presence of horizontally oriented inhibitory interneurons in the superior colliculus. Furthermore, these findings are consistent with the hypothesis that an intrinsic circuit, routed through interneurons, might account for the reciprocal inhibition observed among fixation and saccade-related neurons.

Altered spectral localization cues disrupt the development of the auditory space map in the superior colliculus of the ferret.

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 space was severely degraded at both sound levels. In contrast to normal ferrets, many units had bilobed azimuthal response profiles, indicating that they were unable to resolve sound locations on either side of the interaural axis. There was also much less order in the distribution of best azimuths or elevations of those units that were tuned to a single direction. Some units were tuned to locations that extended much further into the hemifield ipsilateral to the recording side than the normal range of best azimuths. Unilateral removal of the outer ear, which disrupts the monaural spectral cues for one side only, had a much smaller effect on the development of the auditory representation. At supra- and near-threshold sound levels, the representation of sound azimuth in the SC on both sides of the brain was less scattered than that found after bilateral pinna removal. Nevertheless, units with bilobed responses, broader tuning, and inappropriate best azimuths were observed in both the left and right SC of ferrets in which the left pinna and concha had been removed in infancy. These data illustrate that the localization cues provided by the outer ear play a critical role in the development of the auditory space map in the SC. In contrast to other manipulations of either auditory or visual inputs, the map does not appear to adapt to the changes in spectral cues brought about by pinna removal, suggesting that residual binaural cues are, by themselves, insufficient for its normal maturation.

Auditory brainstem projections to the ferret superior colliculus: Anatomical contribution to the neural coding of sound azimuth

The mammalian superior colliculus (SC) contains a neural map of auditory space. It is not known whether this topographic representation emerges at the level of the SC or is relayed there from other auditory areas. We have used retrograde labelling techniques in ferrets to examine the sources and pattern of innervation from auditory brainstem nuclei. After multiple injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the SC, the heaviest concentrations of labelled cells were found in the nucleus of the brachium (BIN) and external nucleus of the inferior colliculus, with much weaker labelling in the nucleus sagulum, dorsal, intermediate and ventral nuclei of the lateral lemniscus, paralemniscal regions, and periolivary nuclei. The projections were predominantly ipsilateral, although labelled cells were found on both sides of the brainstem. Single injections of WGA-HRP or discrete injections of red and green latex microspheres revealed that the caudal and lateral regions of the SC receive the heaviest projections, although the majority of the retrogradely labelled neurons in the contralateral BIN project to rostral SC. On the ipsilateral side, neurons in rostral and caudal regions of the BIN were labelled primarily by the tracer injected into rostral and caudal regions of the SC, respectively. However, no clear segregation was apparent in the BIN after injections into the medial and lateral regions or in any of the other nuclei after either injection paradigm. These data suggest that converging inputs from several auditory brainstem nuclei contribute to the construction of the auditory space map in the SC, although information about sound azimuth may be conveyed to this nucleus via a spatially ordered projection from the ipsilateral BIN. J. Comp. Neurol. 390:342–365, 1998. © 1998 Wiley-Liss, Inc.

Auditory brainstem projections to the ferret superior colliculus: Anatomical contribution to the neural coding of sound azimuth

The mammalian superior colliculus (SC) contains a neural map of auditory space. It is not known whether this topographic representation emerges at the level of the SC or is relayed there from other auditory areas. We have used retrograde labelling techniques in ferrets to examine the sources and pattern of innervation from auditory brainstem nuclei. After multiple injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the SC, the heaviest concentrations of labelled cells were found in the nucleus of the brachium (BIN) and external nucleus of the inferior colliculus, with much weaker labelling in the nucleus sagulum, dorsal, intermediate and ventral nuclei of the lateral lemniscus, paralemniscal regions, and periolivary nuclei. The projections were predominantly ipsilateral, although labelled cells were found on both sides of the brainstem. Single injections of WGA-HRP or discrete injections of red and green latex microspheres revealed that the caudal and lateral regions of the SC receive the heaviest projections, although the majority of the retrogradely labelled neurons in the contralateral BIN project to rostral SC. On the ipsilateral side, neurons in rostral and caudal regions of the BIN were labelled primarily by the tracer injected into rostral and caudal regions of the SC, respectively. However, no clear segregation was apparent in the BIN after injections into the medial and lateral regions or in any of the other nuclei after either injection paradigm. These data suggest that converging inputs from several auditory brainstem nuclei contribute to the construction of the auditory space map in the SC, although information about sound azimuth may be conveyed to this nucleus via a spatially ordered projection from the ipsilateral BIN.

Sources of subcortical projections to the superior colliculus in the ferret

We have identified brainstem and other subcortical afferents to the superior colliculus (SC) in the ferret, by examining the pattern of retrograde labelling that resulted from unilateral injections of red and green fluorescent latex microspheres or of wheat germ agglutinin conjugated to horseradish peroxidase into different regions of this midbrain nucleus. Labelled neurons were found in many structures, including somatosensory, visual and auditory nuclei. These subcortical inputs are almost all bilateral, although most are primarily ipsilateral. Despite some differences in organization, the subcortical projections to the ferret SC broadly resemble those described in other species. Following injections of red and green microspheres in either the rostral and caudal or the medial and lateral regions of the SC, double-labelled cells usually accounted for less than 10% of the total number of retrogradely labelled cells, indicating that most of the subcortical neurons project to discrete regions of the SC. Many of these afferents show some topographic organization, which is much more evident along the rostrocaudal axis of the SC than in the medial-lateral dimension. The intercollicular projection is restricted mainly to the rostral SC and demonstrates a point-to-point organization. Most of the subcortical structures caudal to the central region of the SC were labelled mainly by the tracers injected in caudal SC, while those rostral to this region, including the zona incerta and the pretectal nuclei, were labelled largely by injections in rostral SC. These findings suggest that projections originating from nuclei posterior to the central region of the SC terminate principally in caudal SC whereas afferents from structures anterior to the central region project largely to rostral SC.

Topographic organization of projection from the parabigeminal nucleus to the superior colliculus in the ferret revealed with fluorescent latex microspheres

Unilateral, discrete injections of red and green fluorescent latex microspheres or injections of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) were made into the ferret's superior colliculus (SC) to characterize the topographic organization of the projection from the parabigeminal nucleus (PBN). Retrograde labelling in the PBN revealed that this nucleus projects bilaterally to the SC, although the heaviest projection arises from the ipsilateral PBN. The PBN-SC projection demonstrates a highly ordered organization along the rostral-caudal axis; rostral PBN projects to rostral SC and caudal PBN projects to caudal SC. The caudoventral and rostrodorsal areas of the PBN project mainly to the ipsilateral and contralateral SC, respectively. The ipsilateral pathway terminates principally in the caudal region of the SC, while the contralateral projection terminates predominantly in rostral SC. Ipsilaterally, there are slightly more neurons, located mainly in the ventral PBN, that project to the lateral SC than those, located largely in the dorsal part of the nucleus, that target the medial SC. The contralateral PBN mainly projects to the rostrolateral quadrant of the SC. These results indicate that each quadrant of the SC is innervated principally by a restricted part of the PBN: the caudolateral quadrant, which receives the heaviest ipsilateral input, and the caudomedial quadrant are targeted predominantly by the ventral and dorsal portions, respectively, of the ipsilateral PBN; the rostrolateral quadrant by the contralateral PBN, and the rostromedial quadrant, which receives the weakest input, by the dorsal portion of the nucleus on both sides. These findings suggest that activity in the PBN is relayed to distinct regions of the SC in the form of a highly ordered topographic projection. The adjacent lateral tegmentum (ALT) also projects heavily to the SC, principally on the ipsilateral side. The ALT projection to the ipsilateral SC appears to be organized in a less orderly fashion, and terminates principally in caudal SC, particularly the caudolateral quadrant. No topography was apparent for the contralateral projection.

Chapter 24 The development of topographically-aligned maps of visual and auditory space in the superior colliculus

The role of the superior colliculus in attending and orienting to sensory stimuli is facilitated by the presence within this midbrain nucleus of superimposed maps of different sensory modalities. We have studied the steps involved in the development of topographically-aligned maps of visual and auditory space in the ferret superior colliculus. Injections of fluorescent beads into the superficial layers showed that the projection from the contralateral retina displays topographic order on the day of birth (PO). Recordings made from these layers at the time of eye opening, approximately 1 month later, revealed the presence of an adult-like map of visual space. In contrast, the auditory space map in the deeper layers emerged gradually over a much longer period of postnatal life. In adult ferrets in which one eye had been deviated laterally just before eye opening, the auditory spatial tuning of single units recorded in the contralateral superior colliculus was shifted by a corresponding amount, so that the registration of the visual and auditory maps was maintained. Chronic application of the NMDA-receptor antagonist MK801 disrupted the normal development of the auditory space map, but had no effect on the visual map in either juvenile or adult animals, or on the auditory map once it had matured. These findings indicate that visual cues may play an instructive role, possibly via a Hebbian mechanism of synaptic plasticity, in the development of appropriately tuned auditory responses, thereby ensuring that the neural representations of both modalities share the same coordinates. Changes observed in the auditory representation following partial lesions of the superficial layers at PO suggest that these layers may provide the source of the visual signals responsible for experience-induced plasticity in auditory spatial tuning.

Responses of neurons in the ferret superior colliculus to the spatial location of tonal stimuli

Using multi-unit recordings, we compared the azimuthal spatial selectivity of auditory neurons in the deep layers of the ferret superior colliculus (SC) to broadband and tonal stimuli. Responses to noise were tuned at different sound levels to a single location, which varied topographically along the rostrocaudal axis of the nucleus to form a map of sound azimuth. Frequency response profiles tended to be multi-peaked, so the spatial tuning was examined at two or more frequencies in each case. Some of the azimuthal response profiles obtained with tonal stimuli were bilobed, as expected from the spatially ambiguous cues available at individual frequencies, although the rest were tuned to a single region of space. The preferred sound directions usually varied with the frequency used, and the range of auditory best positions at each recording site was significantly greater with tones than with noise. Comparison with the acoustical properties of the auditory periphery suggested that the near-threshold positional selectivity of many of the tonal responses may be determined by the monaural directionality of the outer ear. When the sound level was raised by 20 dB so that both ears were stimulated at all speaker locations, the range of tonal best positions obtained at each frequency increased and some of the units responded best to pure tones located in the ipsilateral hemifield. The lack of topographic order in the distribution of tonal spatial selectivity along the rostrocaudal axis of the SC indicates the need for a broadband input, incorporating the spectral localization cues provided by the outer ear, in the construction of a neural map of auditory space.

The cholinergic input to the superficial layers of the superior colliculus: an ultrastructural immunocytochemical study in the ferret

The cholinergic innervation of the superficial layers of the ferret's superior colliculus was investigated with a combination of electron microscopy and choline acetyltransferase immunohistochemistry. Cholinergic boutons in the superficial layers of the superior colliculus possess spherical vesicles and make predominantly asymmetrical synapses onto the profiles of small dendrites, as do the terminals of cortical and retinal axons. In most areas of the brain studied so far, cholinergic terminals tend to form synapses of the symmetrical variety.