Experimentally induced visual projections into auditory thalamus and cortex

Retinal cells have been induced to project into the medial geniculate nucleus, the principal auditory thalamic nucleus, in newborn ferrets by reduction of targets of retinal axons in one hemisphere and creation of alternative terminal space for these fibers in the auditory thalamus. Many cells in the medial geniculate nucleus are then visually driven, have large receptive fields, and receive input from retinal ganglion cells with small somata and slow conduction velocities. Visual cells with long conduction latencies and large contralateral receptive fields can also be recorded in primary auditory cortex. Some visual cells in auditory cortex are direction selective or have oriented receptive fields that resemble those of complex cells in primary visual cortex. Thus, functional visual projections can be routed into nonvisual structures in higher mammals, suggesting that the modality of a sensory thalamic nucleus or cortical area may be specified by its inputs during development.     

Visual and nonvisual auditory systems in mammals. Anatomical evidence indicates two kinds of auditory pathways and suggests two kinds of hearing in mammals

Examination of the structural organization of the auditory system of the brain stem shows that the system is composed of a number of separate ascending pathways. This suggests that there may be at least two auditory systems, analogous to the rod and cone pathways in vision. We examined this possibility by investigating the variation in relative size of the medial and lateral superior olivary nuclei in a number of different mammalian species. The lateral superior olive is present in the hedgehog (an insectivore), cat (acarnivore), and squirrel monkey a(primate), but the medial superior olive is absent in the hedgehog. In a group of animals of the same taxonomic order (rodents) the lateral superior olive was present in all species examined, but the medial superior olive was almost wholly absent in the mouse and very prominent in the chinchilla and guinea pig. The absence of the medial superior olive in some animals is surprising because recent anatomical and physiological work has implicated the nucleus in auditory localization. Because of this implication, the medial and lateral olivary nuclei were examined in three species of bat and one dolphin, all echolocating animals. The medial superior olive was absent in these animals, and the lateral superior olive was prominent. These observations support the idea that the medial and lateral superior olives are nuclei on two different ascending auditory systems. It was also noted that the medial superior olive was always well developed in animals with well-developed eyes, and this suggested that the nucleus is in some way related to the visual system. We examined this idea by studying the relation between the numbers of cells in the medial superior olive and in the nucleus of the 6th cranial nerve (one of the motor nuclei concerned with eye movement) in a number of mammalian species. An approximately linear function was found between the sizes of the 6th nucleus and of the medial superior olive in three primates with cone-cell retinas (squirrel monkey, man, and macaque) and four rodents with rod-cell retinas (mouse, rat, guinea pig, and chinchilla). The cell numbers for the ground squirrel (a rodent with cone-cell retina) fitted an extension of the primate curve, and the cell numbers for the cat (in whose retina rods predominate) fitted an extension of the rodent curve. Thus, it is clear that the medial superior olive is related to the visual system, and that it is present in animals with cone-cell fovea and retina (diurnalanimals) and animals with rod-cell retina (that is, nocturnal animals) having good vision. In nonvisual nocturnal animals the nucleus is small or absent. The medial superior olive is probably not concerned with auditory localization in the psychophysical sense but is probably concerned with the movement of head and eyes in the direction of a sound in space. Localization in the psychophysical sense and fine auditory discrimination probably depend upon the ascending pathway which includes the lateral superior olive.     

Functional mapping of the primate auditory system

Cerebral auditory areas were delineated in the awake, passively listening, rhesus monkey by comparing the rates of glucose utilization in an intact hemisphere and in an acoustically isolated contralateral hemisphere of the same animal. The auditory system defined in this way occupied large portions of cerebral tissue, an extent probably second only to that of the visual system. Cortically, the activated areas included the entire superior temporal gyrus and large portions of the parietal, prefrontal, and limbic lobes. Several auditory areas overlapped with previously identified visual areas, suggesting that the auditory system, like the visual system, contains separate pathways for processing stimulus quality, location, and motion.     

Vision guides the adjustment of auditory localization in young barn owls

Barn owls raised with one ear plugged make systematic errors in auditory localization when the earplug is removed. Young owls correct their localization errors within a few weeks. However, such animals did not correct their auditory localization errors when deprived of vision. Moreover, when prisms were mounted in front of their eyes, they adjusted their auditory localization to match the visual error induced by the prisms, as long as the visual and auditory errors were within the same quadrant of directions. The results demonstrate that, during development, the visual system provides the spatial reference for fine-tuning auditory localization.     

Auditory pathways to the frontal cortex of the mustache bat, Pteronotus parnellii

In primates, certain areas of the frontal cortex play a role in guiding movements toward visual or auditory objects in space. The projections from auditory centers to the frontal cortex of the bat Pteronotus parnellii were examined because echolocating bats utilize auditory cues to guide their movements in space. An area in the frontal cortex receives a direct projection from a division of the auditory thalamus, the suprageniculate nucleus, which in turn receives input from the anterolateral peri-olivary nucleus, an auditory center in the medulla. This pathway to the frontal cortex bypasses the main auditory centers in the midbrain and cortex and could involve as few as four neurons between the cochlea and the frontal cortex. The auditory cortex is also a major source of input to the frontal cortex. This area of the frontal cortex may link the auditory and motor systems by its projections to the superior colliculus.     

Auditory association cortex lesions impair auditory short-term memory in monkeys

Monkeys that were trained to perform auditory and visual short-term memory tasks (delayed matching-to-sample) received lesions of the auditory association cortex in the superior temporal gyrus. Although visual memory was completely unaffected by the lesions, auditory memory was severely impaired. Despite this impairment, all monkeys could discriminate sounds closer in frequency than those used in the auditory memory task. This result suggests that the superior temporal cortex plays a role in auditory processing and retention similar to the role the inferior temporal cortex plays in visual processing and retention.     

Visual instruction of the neural map of auditory space in the developing optic tectum

Neural maps of visual and auditory space are aligned in the adult optic tectum. In barn owls, this alignment of sensory maps was found to be controlled during ontogeny by visual instruction of the auditory spatial tuning of neurons. Large adaptive changes in auditory spatial tuning were induced by raising owls with displacing prisms mounted in spectacle frames in front of the eyes; neurons became tuned to sound source locations corresponding to their optically displaced, rather than their normal, visual receptive field locations. The results demonstrate that visual experience during development calibrates the tectal auditory space map in a site-specific manner, dictating its topography and alignment with the visual space map.     

A map of visual space induced in primary auditory cortex

Maps of sensory surfaces are a fundamental feature of sensory cortical areas of the brain. The relative roles of afferents and targets in forming neocortical maps in higher mammals can be examined in ferrets in which retinal inputs are directed into the auditory pathway. In these animals, the primary auditory cortex contains a systematic representation of the retina (and of visual space) rather than a representation of the cochlea (and of sound frequency). A representation of a two-dimensional sensory epithelium, the retina, in cortex that normally represents a one-dimensional epithelium, the cochlea, suggests that the same cortical area can support different types of maps. Topography in the visual map arises both from thalamocortical projections that are characteristic of the auditory pathway and from patterns of retinal activity that provide the input to the map.     

Auditory frequency-following response: neural or artifact?

An electrical response which reproduces the waveform and frequency of the sound stimulus can be recorded from the central neural pathway for audition. Controversy has existed for some years over whether this frequency-following response (FFR) is neural or an artifact such as remote pickup of the cochlear microphonic or cross talk in the recording system. Two experiments resolve this issue by demonstrating that the frequency-following response depends upon functionally intact neural pathways. The frequency-following response, as well as auditory evoked potentials, is abolished by section of the eighth nerve; it is reversibly abolished by cooling of the cochlear nucleus.     

A neural map of auditory space in the owl

Auditory units that responded to sound only when it originated from a limited area of space were found in the lateral and anterior portions of the midbrain auditory nucleus of the owl (Tyto alba). The areas of space to which these units responded (their receptive fields) were largely independent of the nature and intensity of the sound stimulus. The units were arranged systematically within the midbrain auditory nucleus according to the relative locations of their receptive fields, thus creating a physiological map of auditory space.     

Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina

The development of orderly connections in the mammalian visual system depends on action potentials in the optic nerve fibers, even before the retina receives visual input. In particular, it has been suggested that correlated firing of retinal ganglion cells in the same eye directs the segregation of their synaptic terminals into eye-specific layers within the lateral geniculate nucleus. Such correlations in electrical activity were found by simultaneous recording of the extracellular action potentials of up to 100 ganglion cells in the isolated retina of the newborn ferret and the fetal cat. These neurons fired spikes in nearly synchronous bursts lasting a few seconds and separated by 1 to 2 minutes of silence. Individual bursts consisted of a wave of excitation, several hundred micrometers wide, sweeping across the retina at about 100 micrometers per second. These concerted firing patterns have the appropriate spatial and temporal properties to guide the refinement of connections between the retina and the lateral geniculate nucleus.     

Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents

In the adult mammalian visual system, ganglion cell axons from the two eyes are segregated from each other into separate layers within their principal target, the lateral geniculate nucleus. The involvement of spontaneously generated action potential activity in the process of segregation was investigated during the fetal period in which segregation normally occurs in the cat, between embryonic day 45 (E45) and birth (E65). Tetrodotoxin, which blocks the voltage-sensitive sodium channel, was used to prevent action potentials. Fetuses received continuous intracranial infusions of tetrodotoxin from osmotic minipumps implanted in utero on E42. After a 2-week infusion, intraocular injections of anterograde tracers revealed that tetrodotoxin prevented segregation. The contralateral projection filled the lateral geniculate nucleus uniformly, and the ipsilateral projection expanded to occupy most of what would normally be contralaterally innervated layer A. Thus, in the fetus, long before the onset of vision, spontaneous action potential activity is likely to be present in the visual system and to contribute to the segregation of the retinogeniculate pathway.     

Space perception in early infancy: perception within a common auditory-visual space

Infants as young as 30 days become visibly distressed upon observing their mothers speak to them while the mother's voice is displaced in space. Their ability to perceive this discrepancy indicates that infant perception occurs within a space that is common to the visual and auditory modes.     

Development of polysensory responses in association cortex of kitten

Sensory responsiveness of single neurons in posterior association cortex of kittens that were 7 to 50 days old was investigated. The percentage of trimodal cells (that is, cells that respond to visual, auditory, and somesthetic stimulation) increased gradually until day 50, when percentages of trimodally responsive cells approached the adult level. In the youngest kittens, cells were predominantly responsive to only visual stimulation. With maturation, responsiveness to auditory and then to somesthetic stimulation was observed in increasing percentages of cells.     

Self-stimulation alters human sensory brain responses

Human electrocortical potentials evoked by self-administered auditory and visual stimuli manifest much smaller amplitude and faster poststimulus timing than do average brain responses evoked by identical machine-delivered stimuli. Auditory evoked potentials show this "self-stimulation effect" to a greater degree than do visual responses. For visual evoked potentials, the effect appears greater at the vertex association area than over the occipital cortex. Individual differences in the magnitude of the "self-stimutlation effect" relate to level of intelligence.     

Neurons generated in the adult brain are recruited into functional circuits

Adult canaries, Serinus canarius, received injections of 3H-labeled thymidine, a marker of DNA synthesis. Thirty days after the last injection, intracellular potentials were recorded from neurons in the nucleus hyperstriatum ventralis pars caudalis, a vocal control nucleus in the telencephalon; these same cells were then injected with horseradish peroxidase. Of the 74 neurons labeled with horseradish peroxidase that were recovered, the nuclei of seven were radioactively labeled. Four of these seven neurons had responded to auditory stimuli. These double-labeled neurons were apparently generated during or after the 3H-labeled thymidine treatment (during adulthood) and subsequently incorporated into functional neural circuits.     

Delayed Visual Feedback and Behavior

By means of video-tape recording the visual presentation of a person's behavior as he carries out some task, can be delayed in such a way that the individual sees what he is doing a short time after he has done it. The effects of this delay of visual feedback on a variety of simple visual-motor tasks are found to be both marked and deleterious, and in some respects similar to the effects of delayed auditory feedback on speech and motor tasks.     

Visibility of comet nuclei

Photography of the nucleus of comet Halley is the goal of several planned space missions. The nucleus of a comet is surrounded by a cloud of dust particles. If this cloud is optically thick, it will prevent observation of the nuclear surface. Broadband photometry of nine comets has been analyzed to determine the visibility of their nuclei. Only in the case of comet West near perihelion was the dust dense enough to interfere with imaging. Comparison of the visual brightness of the well-observed comets with that of Halley in 1910 leads to the conclusion that the nucleus of Halley can be imaged without significant obscuration by the dust.     

Auditory midbrain responses parallel spectral integration phenomena

Resolving the frequency components of complex sound spectra including speech is an inherent, important accomplishment of the auditory nervous systems of vertebrates. The critical perceptual unit in the frequency domain, the critical bandwidth, has a simple functional equivalent within the principal midbrain auditory nucleus--the central nucleus of the inferior colliculus.     

Superior colliculus: some receptive field properties of bimodally responsive cells

Many cells in the intermediate and deep gray layers of the superior colliculus of the cat respond to both auditory and visual stimuli. These cells have similar receptive fields for both modalities and are directionally selective for both modalities, requiring stimuli moving laterally away from the animal. Perhaps cells that integrate auditory and visual information participate in the control of orienting and following responses to stimuli of both modalities.