Nobuo Suga

Multiparametric corticofugal modulation and plasticity in the auditory system

The auditory systems of adult animals can be reorganized by auditory experience. The auditory cortex, the corticofugal system and the cholinergic basal forebrain are crucial for this reorganization. The auditory system can undergo two different forms of reorganization — expansion and compression. Whereas expanded reorganization has been found in different species and different sensory systems, compressed reorganization has only been found in the auditory system of the moustached bat, which is highly specialized for echolocation. Here, we review recent progress in our understanding of the corticofugal system and the reorganization of the auditory system.

Corticofugal modulation of frequency processing in bat auditory system

Auditory signals are transmitted from the inner ear through the brainstem to the higher auditory regions of the brain. Neurons throughout the auditory system are tuned to stimulus frequency, and in many auditory regions are arranged in topographical maps with respect to their preferred frequency. These properties are assumed to arise from the interactions of convergent and divergent projections ascending from lower to higher auditory areas; such a view, however, ignores the possible role of descending projections from cortical to subcortical regions. In the bat auditory system, such corticofugal connections modulate neuronal activity to improve the processing of echo-delay information,, a specialized feature. Here we show that corticofugal projections are also involved in the most common type of auditory processing, frequency tuning. When cortical neurons tuned to a specific frequency are inactivated, the auditory responses of subcortical neurons tuned to the same frequency are reduced. Moreover, the responses of other subcortical neurons tuned to different frequencies are increased, and their preferred frequencies are shifted towards that of the inactivated cortical neurons. Thus the corticofugal system mediates a positive feedback which, in combination with widespread lateral inhibition, sharpens and adjusts the tuning of neurons at earlier stages in the auditory processing pathway.

Cortical computational maps for auditory imaging

Abstract The mustached bat emits complex biosonar signals (pulses) and listens to echoes for orientation and hunting flying insects. Different types of biosonar information are conveyed by different parameters characterizing pulse-echo pairs. For example, range information is conveyed by echo delay, while velocity information is carried by Doppler shift. At the auditory periphery, frequency is expressed by the anatomical location along the basilar membrane and also along the array of ganglion cells, while amplitude and time (duration of signals and interval between signals) are not expressed by anatomical locations, but by discharge rate and the temporal pattern of nerve discharges, respectively. In the auditory cortex, however, not only frequency but also other information-bearing parameters (IBPs) such as echo delay and Doppler shift are systematically expressed by anatomical locations. That is, the IBPs are mapped. These computational maps greatly depend upon subcortical signal processing. The subcortical auditory nuclei create delay lines and multipliers (or AND gates) for processing range (echo delay) information, and also create level-tolerant frequency tuning and multipliers (or AND gates) for processing velocity (Doppler shift) information. These multipliers are called FM-FM or CF/CF combination-sensitive neurons, respectively. Signal processing in the auditory system is parallel-hierarchical. The neurophysiological studies of the bats auditory system provide an excellent data base for computational models.

Corticofugal Modulation of Time-Domain Processing of Biosonar Information in Bats

The Jamaican mustached bat has delay-tuned neurons in the inferior colliculus, medial geniculate body, and auditory cortex. The responses of these neurons to an echo are facilitated by a biosonar pulse emitted by the bat when the echo returns with a particular delay from a target located at a particular distance. Electrical stimulation of cortical delay-tuned neurons increases the delay-tuned responses of collicular neurons tuned to the same echo delay as the cortical neurons and decreases those of collicular neurons tuned to different echo delays. Cortical neurons improve information processing in the inferior colliculus by way of the corticocollicular projection.

Corticofugal modulation of the midbrain frequency map in the bat auditory system.

The auditory system, like the visual and somatosensory systems, contains topographic maps in its central neural pathways. These maps can be modified by sensory deprivation, injury and experience in both young and adult animals. Such plasticity has been explained by changes in the divergent and convergent projections of the ascending sensory system. Another possibility, however, is that plasticity may be mediated by descending corticofugal connections. We have investigated the role of descending connections from the cortex to the inferior colliculus of the big brown bat. Electrical stimulation of the auditory cortex causes a downward shift in the preferred frequencies of collicular neurons toward that of the stimulated cortical neurons. This results in a change in the frequency map within the colliculus. Moreover, similar changes can be induced by repeated bursts of sound at moderate intensities. Thus, one role of the mammalian corticofugal system may be to modify subcortical sensory maps in response to sensory experience.

Plasticity and Corticofugal Modulation for Hearing in Adult Animals

The descending (corticofugal) auditory system adjusts and improves auditory signal processing in the subcortical auditory nuclei. The auditory cortex and corticofugal system evoke small, short-term changes of the subcortical auditory nuclei in response to a sound repetitively delivered to an animal. These changes are specific to the parameters characterizing the sound. When the sound becomes significant to the animal through conditioning (associative learning), the changes are augmented and the cortical changes become long-term. There are two types of reorganizations: expanded reorganization resulting from centripetal shifts in tuning curves of neurons toward the values of the parameters characterizing a sound and compressed reorganization resulting from centrifugal shifts in tuning curves of neurons away from these values. The two types of reorganizations are based on a single mechanism consisting of two components: facilitation and inhibition.

Neural Attenuation of Responses to Emitted Sounds in Echolocating Bats

Bats of the family Vespertilionidae enmit strong ultrasonic pulses for echolocation. If such sounds directly stimulate their ears, the detection of echoes from short distances would be impaired. The responses of lateral lemniscal neurons to emitted sounds were found to be much smaller than those to playback sounds, even when the response of the auditory nerve was the same to both types of sounds. Thus, responses to self-vocalized sounds were attenuated between the cochlear nerve and the inferior colliculus. The mean attenuation was 25 decibels. This neural attenuating mechanism is probably a part of the mechanisms for effective echo detection.

Modulation of cochlear hair cells by the auditory cortex in the mustached bat.

The corticofugal (descending) auditory system forms multiple feedback loops, and adjusts and improves auditory signal processing in the subcortical auditory nuclei. However, the mechanism by which the corticofugal system modulates cochlear hair cells has been unexplored. We found that electric stimulation of cortical neurons via the corticofugal system modulates cochlear hair cells in a highly specific way according to the relationship in terms of best frequency between cortical neurons and hair cells. Such frequency-specific effects can be explained by selective corticofugal modulation of individual olivocochlear efferent fibers.The corticofugal (descending) auditory system forms multiple feedback loops, and adjusts and improves auditory signal processing in the subcortical auditory nuclei. However, the mechanism by which the corticofugal system modulates cochlear hair cells has been unexplored. We found that electric stimulation of cortical neurons via the corticofugal system modulates cochlear hair cells in a highly specific way according to the relationship in terms of best frequency between cortical neurons and hair cells. Such frequency-specific effects can be explained by selective corticofugal modulation of individual olivocochlear efferent fibers.

Cortical computational maps control auditory perception

Mustached bats orient and find insects by emitting ultrasonic pulses and analyzing the returning echoes. Neurons in the Doppler-shifted constant-frequency (DSCF) and frequency-modulated (FM-FM) areas of the auditory cortex form maps of echo frequency (target velocity) and echo delay (target range), respectively. Bats were trained to discriminate changes in echo frequency or delay, and then these areas were selectively inactivated with muscimol. Inactivation of the DSCF area disrupted frequency but not delay discriminations; inactivation of the FM-FM area disrupted delay but not frequency discriminations. Thus, focal inactivation of specific cortical maps produces specific disruptions in the perception of biosonar signals.

Role of corticofugal feedback in hearing

The auditory system consists of the ascending and descending (corticofugal) systems. The corticofugal system forms multiple feedback loops. Repetitive acoustic or auditory cortical electric stimulation activates the cortical neural net and the corticofugal system and evokes cortical plastic changes as well as subcortical plastic changes. These changes are short-term and are specific to the properties of the acoustic stimulus or electrically stimulated cortical neurons. These plastic changes are modulated by the neuromodulatory system. When the acoustic stimulus becomes behaviorally relevant to the animal through auditory fear conditioning or when the cortical electric stimulation is paired with an electric stimulation of the cholinergic basal forebrain, the cortical plastic changes become larger and long-term, whereas the subcortical changes stay short-term, although they also become larger. Acetylcholine plays an essential role in augmenting the plastic changes and in producing long-term cortical changes. The corticofugal system has multiple functions. One of the most important functions is the improvement and adjustment (reorganization) of subcortical auditory signal processing for cortical signal processing.