Post-crucial Period Effects of Auditory Experience and Deprivation on the Guinea-pig Superior Collicular Map of Auditory Space.

A four-day period of bimodality auditory and visual experience is sufficient to permit normal emergence of the map of auditory space in the guinea pig superior colliculus

Neurotransmitter involvement in development and maintenance of the auditory space map in the guinea pig superior colliculus. J. Neurophysiol. 80: 2941-2953, 1998. The mammalian superior colliculus (SC) is a complex area of the midbrain in terms of anatomy, physiology, and neurochemistry. The SC bears representations of the major sensory modalites integrated with a motor output system. It is implicated with saccade generation, in behavioral responses to novel sensory stimuli and receives innervation from diverse regions of the brain using many neurotransmitter classes. Ethylene-vinyl acetate copolymer (Elvax-40W polymer) was used here to deliver chronically neurotransmitter receptor antagonists to the SC of the guinea pig to investigate the potential role played by the major neurotransmitter systems in the collicular representation of auditory space. Slices of polymer containing different drugs were implanted onto the SC of guinea pigs before the development of the SC azimuthal auditory space map, at approximately 20 days after birth (DAB). A further group of animals was exposed to aminophosphonopentanoic acid (AP5) at approximately 250 DAB. Azimuthal spatial tuning properties of deep layer multiunits of anesthetized guinea pigs were examined approximately 20 days after implantation of the Elvax polymer. Broadband noise bursts were presented to the animals under anechoic, free-field conditions. Neuronal responses were used to construct polar plots representative of the auditory spatial multiunit receptive fields (MURFs). Animals exposed to control polymer could develop a map of auditory space in the SC comparable with that seen in unimplanted normal animals. Exposure of the SC of young animals to AP5, 6-cyano-7-nitroquinoxaline-2,3-dione, or atropine, resulted in a reduction in the proportion of spatially tuned responses with an increase in the proportion of broadly tuned responses and a degradation in topographic order. Thus N-methyl--aspartate (NMDA) and non-NMDA glutamate receptors and muscarinic acetylcholine receptors appear to play vital roles in the development of the SC auditory space map. A group of animals exposed to AP5 beginning at approximately 250 DAB produced results very similar to those obtained in the young group exposed to AP5. Thus NMDA glutamate receptors also seem to be involved in the maintenance of the SC representation of auditory space in the adult guinea pig. Exposure of the SC of young guinea pigs to gamma-aminobutyric acid (GABA) receptor blocking agents produced some but not total disruption of the spatial tuning of auditory MURFs. Receptive fields were large compared with controls, but a significant degree of topographical organization was maintained. GABA receptors may play a role in the development of fine tuning and sharpening of auditory spatial responses in the SC but not necessarily in the generation of topographical order of the these responses.

There were two primary aims of this study. First, to observe if the map of auditory space in the superior colliculus (SC) of the guinea-pig could recover after periods of normal visual experience following visual deprivation during the crucial period. Second, to determine whether any degradation of the space map was observed when the animal was visually deprived for different lengths of time after the crucial period. Animals deprived of visual experience during the crucial period and then allowed normal experience did show a limited ability to construct a SC auditory space map. Whereas visual deprivation following normal auditory and visual experience during the crucial period caused a profound degradation, of both spatial tuning and topography, of auditory receptive fields in the SC. Additional data indicate that the SC auditory space map remains vulnerable to visual deprivation until at least 100 days after birth.

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.

The developmental emergence of a map of auditory space in the superior colliculus of the guinea pig

The developmental emergence of the representation of auditory azimuth in the external nucleus of the inferior colliculus of the guinea-pig: the effects of visual and auditory deprivation

In the guinea-pig the development and maintenance of the superior collicular (SC) auditory space map requires both auditory and visual experience. This paper reports the results of experiments in which adult animals (of different ages) were dark-reared for 4 weeks to define the extent of the period of susceptibility to visual deprivation of the SC auditory map. Dark-rearing for 4 weeks from 100, 150 or 200 days after birth caused degradation of spatial tuning and topography of multi-unit auditory responses in the SC. In contrast, animals reared in the dark from 250 days after birth showed spatially tuned auditory responses similar to those seen in normal animals. These data suggest that the SC auditory space map in the adult guinea-pig remains susceptible to visual deprivation up to 200 days after birth.

In the normal guinea pig a map of auditory space appears, in the deeper layers of the superior colliculus, at 32 days after birth (DAB). The animal is unable to construct this collicular map of auditory space in the absence of developmental visual experience. Auditory receptive fields of animals dark-reared from birth are typically large, occupying most of the contralateral hemifield. There is no topographic relationship between the collicular location of the recording electrode and the spatial position from which auditory stimuli elicit a maximal response. The fields of dark-reared animals resemble, in their tuning parameters, the spatially undifferentiated fields typical of young postnatal normal guinea pigs. To investigate the time-course during which visual experience is required for map emergence, animals received normal visual experience until either 18 or 26 DAB and were then dark-reared until the terminal mapping experiment. Maps developed in neither group. Animals provided with a normal visual environment until 30 DAB, and then placed in the dark did, however, construct topographically organized spatial maps with discrete spatial receptive fields. Maps also failed to emerge in animals receiving normal visual experience both before and after a 4-day period of visual deprivation between 26 and 30 DAB. We conclude that this 4-day period, or part of it, constitutes a 'crucial' period during which visual experience is required for the normal elaboration of the collicular map of auditory space.

Previous data have indicated that, if guinea pigs are deprived of all visual information during a crucial period early in development (26-30 days after birth), the map of auditory space in the superior colliculus (SC) is completely disrupted. In the experiments reported here, multi-unit auditory receptive fields were recorded in the SC of two groups of anaesthetised guinea pigs that had been exposed to different forms of visual deprivation. One group was reared in a movement-free environment (strobe-reared) and the other group was reared in a pattern-free environment (their eyes covered with light-diffusing masks). Both groups experienced visual restriction during the crucial period for auditory space map development. In both experimental groups, the multi-unit auditory receptive fields were broad and all spatial tuning parameter values were significantly greater than the equivalent values from a control group of normal animals. In the pattern- and motion-deprived groups, a significant correlation existed between the rostro-caudal position of the recording electrode in the SC and the peak response angle of the receptive field, thus showing a degree of topographic organisation of the auditory receptive fields in the SC. However, the topographic order was less precise than that displayed by the control group of animals. These results indicate that, during development, both visual pattern and movement are important for the refinement of the SC auditory space map in the guinea pig.

The aims of this study were to determine whether electrode discrimination by early-deafened subjects using the Cochlear Limited prosthesis varied at different locations on the electrode array, was influenced by the effects of auditory deprivation and experience with electric stimulation, and was related to speech perception. Difference limens for electrode discrimination were measured in 16 early-deafened subjects at three positions on the array: electrodes 18 (apical), 14 (mid), and 8 (basal). Electrodes were stimulated using random variations in current level to minimize the influence of loudness cues. Assessed were correlations between the difference limens, subject variables related to auditory deprivation (age at onset of deafness, duration of deafness, and age at implantation) and auditory experience (duration of implant use and the total time period of auditory experience), and speech perception scores from two closed-set and two open-set tests. The average difference limens across the three positions were less than two electrodes for 75% of subjects, with average limens between 2 and 6.5 electrodes for the remaining 25% of subjects. Significant differences across the three positions were found for 69% of subjects. The average limens and those at the basal position positively correlated with variables related to auditory deprivation, with larger limens for subjects implanted at a later age and with a longer duration of deafness. The average limens and those at the apical position negatively correlated with closed-set speech perception scores, with lower scores for subjects with larger limens, but not with open-set scores. Speech scores also negatively correlated with variables related to auditory deprivation. These findings showed that early-deafened subjects were generally successful in electrode discrimination although performance varied across the array for over half the subjects. Discrimination performance was influenced by the effects of auditory deprivation, and both electrode discrimination and variables related to auditory deprivation influenced closed-set speech perception.

The role of the external nucleus of the inferior colliculus in the construction of the superior collicular auditory space map in the guinea-pig

The basic wiring of the brain is first established before birth by using a variety of molecular guidance cues. These connections are then refined by patterns of neural activity, which are initially generated spontaneously and subsequently driven by sensory experience. In the superior colliculus, a midbrain nucleus involved in the control of orienting behaviour, visual, auditory, and tactile inputs converge to form superimposed maps of sensory space. Maps of visual space and of the body surface arise from spatially ordered projections from the retina and skin, respectively. In contrast, the map of auditory space is computed within the brain by tuning the neurons to different localization cues that result from the acoustical properties of the head and ears. Establishing and maintaining the registration of the maps in the face of individual differences in the size and relative positions of different sense organs is an activity-dependent process in which the synaptic circuits underlying the auditory representation are modified and calibrated under the influence of both auditory and visual experience. BioEssays 1999;21:900-911.

In the ferret (Mustela putorius) the map of auditory space in the deeper layers of the superior colliculus (SC) matures over a period of several postnatal weeks, a process known to be guided by both visual and auditory experience. The auditory responses are initially very broadly tuned, and gradually become more selective for specific sound locations that coincide with the visual receptive fields recorded in the same region of the SC. To investigate the possible involvement of NMDA-type glutamate receptors in the postnatal development of this auditory representation, we have reared ferrets in which 400 microns thick sheets of the slow-release polymer Elvax, containing the NMDA receptor antagonists MK801 or APV, were placed on the dorsal surface of the SC. The Elvax was implanted on postnatal day (P) 25-27, just before the onset of hearing, and removed 5-6 weeks later, just prior to recording from the SC on around P61-70. In vitro measurements with Elvax containing 3H-MK801 revealed that the amount of drug released declined sharply over the first 10 d and then stabilized at a fairly constant rate for the following 5 weeks. These in vitro data were found to parallel the in vivo release of MK801 from implanted Elvax slices. Diffusion of MK801 from the implant was measured and significant levels were found within 800 microns of the SC surface, suggesting that the action of MK801 was restricted to the superficial and intermediate layers of the nucleus. Extracellular recordings were made from visual and auditory units in the SC in response to free-field stimulation. The visual responses of units recorded in the superficial layers appeared to be unaffected by either of the drug treatments, and formed a normal, adult-like map of visual azimuth along the rostrocaudal axis of the SC in all animals. Most of the auditory single-unit responses recorded at this age in normal, unoperated controls were spatially tuned and topographically organized, although the map of sound azimuth was less precise than that in adult ferrets. Data from age-matched control animals that had been reared with drug-free Elvax implants were not statistically different from the unoperated juvenile ferrets. However, in animals reared with APV or MK801 Elvax implants, there was an increase in the relative numbers of auditory units that were ambiguously tuned to two or more locations.(ABSTRACT TRUNCATED AT 400 WORDS)

Age-related changes in auditory spatial properties of the guinea pig superior colliculus

Somatosensory-Motor Neuronal Activity in the Superior Colliculus of the Primate