Xiaofeng Ma

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.

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.

Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats

Animal sounds, as well as human speech sounds, are characterized by multiple parameters such as frequency, intensity, duration, etc. The central auditory system produces neurons tuned to particular durations and frequencies of sounds emitted by a species. In bats, “duration-tuned” neurons are mostly sensitive to short durations and high frequencies of sounds used for echolocation. They are scattered in the frequency maps of the inferior colliculus and auditory cortex. We found that electric stimulation of cortical duration-tuned neurons modulates collicular duration-tuned neurons in both duration and frequency tuning only when collicular and cortical neurons paired for studies are within ±4 ms in best duration and within ±6 kHz in best frequency. There are four types of modulations: sharpening or broadening of duration tuning, and lengthening or shortening of best duration. Sharpening is observed in “matched” collicular neurons whose best durations are the same as those of stimulated cortical neurons, and it is accompanied by augmentation of the auditory responses at their best durations. The other three types of modulations are observed in “unmatched” collicular neurons whose best durations are different from those of stimulated cortical neurons. Lengthening or shortening of best duration is linearly related to the amount of the difference in best duration between collicular and cortical neurons. Corticofugal modulation is specific and systematic according to relationships in both duration and frequency between stimulated cortical and recorded collicular neurons.

Specific and Nonspecific Plasticity of the Primary Auditory Cortex Elicited by Thalamic Auditory Neurons

The ventral and medial divisions of the medial geniculate body (MGBv and MGBm) respectively are the lemniscal and nonlemniscal thalamic auditory nuclei. Lemniscal neurons are narrowly frequency tuned and provide highly specific frequency information to the primary auditory cortex (AI), whereas nonlemniscal neurons are broadly frequency tuned and project widely to auditory cortical areas including AI. The MGBv and MGBm are presumably different not only in auditory signal processing, but also in eliciting cortical plastic changes. We electrically stimulated MGBv or MGBm neurons and found the following: (1) electric stimulation of narrowly frequency-tuned MGBv neurons evoked the shift of the frequency-tuning curves of AI neurons toward the tuning curves of the stimulated MGBv neurons. This shift was the same as that in the central nucleus of the inferior colliculus and AI elicited by focal electric stimulation of AI or auditory fear conditioning. The widths of the tuning curves of the AI neurons stayed the same or slightly increased. (2) Electric stimulation of broad frequency-tuned MGBm neurons augmented the auditory responses of AI neurons and broadened their frequency-tuning curves which did not shift. These cortical changes evoked by MGBv or MGBm neurons slowly disappeared over 45–60 min after the onset of the electric stimulation. Our findings indicate that lemniscal and nonlemniscal nuclei are indeed different in eliciting cortical plastic changes: the MGBv evokes tone-specific plasticity in AI for adjusting auditory signal processing in the frequency domain, whereas the MGBm evokes nonspecific plasticity in AI for increasing the sensitivity of cortical neurons.

Descending system and plasticity for auditory signal processing: neuroethological data for speech scientists

The auditory system consists of the ascending and descending (corticofugal) systems. One of the major functions of the corticofugal system is the adjustment and improvement of auditory signal processing in the subcortical auditory nuclei, i.e., the adjustment and improvement of the input of cortical neurons. The corticofugal system evokes a small, short-term reorganization (plasticity) of the inferior colliculus, medial geniculate body and auditory cortex (AC) for acoustic signals repetitively delivered to an animal. When these signals become behaviorally relevant to the animal through conditioning (associative learning), the short-term reorganization is augmented and changes into a long-term reorganization of the AC. Mammals may mostly acquire the behavioral relevance of sounds through learning. Human babies may also acquire language through learning. Therefore, the corticofugal system is expected to play an important role in processing behaviorally relevant sounds and in reorganizing the AC according to the behavioral relevance of sounds. Since the ascending and descending systems form multiple feedback loops, the neural mechanisms for auditory information processing cannot be adequately understood without the exploration of the interaction between the ascending and descending systems.