ReviewTuning shifts of the auditory system by corticocortical and corticofugal projections and conditioning
Highlights
► Electric stimulation and conditioning each evoke tone-specific plasticity. ► Pseudo-conditioning evokes nonspecific plasticity of auditory neurons. ► Neural mechanisms for the two types of plasticity are quite different. ► Specialization of the auditory system for plasticity is due to enhanced inhibition. ► A differential gating mechanism exists for auditory signal processing.
Introduction
This article reviews the recent progress in the research of the modulation of the auditory system by corticocortical and corticofugal projections, conditioning and pseudo-conditioning. I will first summarize the anatomical aspects of the auditory system directly related to these physiological studies. The central auditory system is composed of the lemniscal and nonlemniscal pathways or systems. The lemniscal system consists of the central nucleus of the inferior colliculus (ICc), the ventral division of the medial geniculate body (MGBv), the primary auditory cortex (AI) and the anterior auditory field (AAF). It is tonotopically organized. The nonlemniscal system consists of the external (ICx) and dorsal (ICd) nuclei of the IC, the medial (MGBm) and the dorsal (MGBd) divisions of the MGB and the posterior intralaminar nucleus (PIN). It is poorly tonotopically organized. The ICc, ICx and ICd project to the MGBv, MGBm and MGBd, respectively (Aitkin and Webster, 1972, Clarey et al., 1992, Rouiller, 1997 for reviews).
In general, MGBv neurons are sharply frequency-tuned and carry tonotopically organized auditory specific information. Their responses to sounds are consistent. On the contrary, MGBm and MGBd neurons are broadly frequency-tuned and their responses to a repeatedly delivered identical stimulus are inconsistent and quickly habituate. MGBm neurons carry poly-sensory information and are presumably involved in associative learning (Rouiller, 1997, He, 2003, Hu, 2003 for reviews). However, they are sensitive to changes in auditory stimuli (Kraus et al., 1994). The MGBd projects to the cortical auditory areas surrounding AI, whereas the MGBm projects to all auditory areas including AI (Imig and Morel, 1983 for review; Andersen et al., 1980, Winer et al., 1977). Unlike MGBv neurons, MGBm neurons have extensive and direct connections with the amygdala, striatum and association cortex (He, 2003, Hu, 2003 for reviews). Therefore, these two systems are anatomically and physiologically quite different from each other. The cortical auditory areas mutually project, so that they are not simply assigned either the lemniscal or nonlemniscal areas. However, for convenience, AI and the secondary auditory cortex (AII) are included in the lemniscal and nonlemniscal systems, respectively.
The cortical auditory areas project to the corresponding contralateral cortical areas through the corpus callosum, with certain exceptions (Imig and Brugge, 1978, Liu and Suga, 1997). They also project to subcortical auditory nuclei: AI and AAF project back to the MGBv, ICc and ICx; AII to the MGBd and ICd; and all auditory areas to the MGBm. The ICd receiving sparse ascending auditory projections receives a prominent descending projection from AII (Rouiller, 1997 for review; Andersen et al., 1980, Winer et al., 2001). In echolocating bats, the ICd is extremely small, whereas the ICc is very large (Pollak and Casseday, 1989). Unlike the MGBd, the MGBm projects to AI and AAF, and has feedback from them. Therefore, it may be more important than the MGBd in terms of interactions between the lemniscal and nonlemniscal systems. The GABAergic thalamic reticular nucleus (TRN) receives collateral projections from the thalamocortical (Jones, 1975, Crabtree, 1998) and corticothalamic fibers and projects to the neighboring thalamic nuclei (He, 2003, Hu, 2003 for reviews). The TRN may also play an important role in the interaction between the lemniscal and nonlemniscal systems.
The corticofugal (descending) system forms multiple feedback loops with the ascending system. The shortest feedback loop is the thalamo-cortico-thalamic loop, and the longest one is the cochlea-cortico-cochlear (via multiple auditory nuclei) loop. The colliculo-thalamo-cortico-collicular loop has an intermediate length. The changes occurring in the auditory cortex are looped back to the cortex through these multiple feedback loops.
Acoustic stimuli such as trains of 60 dB SPL tone bursts activate the auditory system and may activate the ascending reticular activating system (ARAS). For auditory fear conditioning and pseudo-conditioning, electric leg- or foot-stimulus has often been used as an unconditioned stimulus (US). The US activates not only the somatosensory system, but also the ARAS and brain aversion system (BAS). They evoke arousal and defensive behaviors, respectively. The ARAS and BAS activate the various neuromodulatory systems which broadly project to both the cerebral cortex and subcortical sensory nuclei and play an important role in their activities and organizations (Siegel, 2002, Brandão et al., 2003 for reviews).
Section snippets
Three major types of changes evoked by focal electric stimulation of the lemniscal system
Focal repetitive stimulation with, e.g., a train of 100 nA, 0.2 ms electric pulses of AI, evokes three major types of changes in the responses and tuning curves of cortical neurons neighboring the stimulated ones. Namely, when the recorded neuron is matched in best frequency (BF) to the stimulated one, the response of the “matched” neuron is augmented at its BF and is inhibited at frequencies lower and/or higher than the BF. As a result, its frequency tuning is sharpened. When BF-unmatched, the
Corticofugal modulation: the primary auditory cortex to the subcortical auditory nuclei and to cochlear hair cells
Neural mechanisms for creating the various response properties of auditory neurons and the “computational” maps – maps different from the tonotopic map inherited from the cochlea – in the central auditory system had been explained only by neural interactions in the ascending auditory system (Suga, 1990, Covey and Casseday, 1999 for reviews). However, the findings since 1995 indicate that the corticofugal system plays important roles in shaping the response properties of the neurons and in
Plasticity related to associative and non-associative learning
Tone burst and electric foot-stimuli have been used as conditioned (CS) and unconditioned (US) stimuli, respectively. When the CS and US are paired as CS–US for conditioning, i.e., for associative learning, an animal shows a conditioned behavioral response specific to the CS and its auditory system shows the “tone-specific” plasticity which consists of the facilitation of auditory responses and sharpening of the frequency tuning of BF-matched neurons and the BF shifts of BF-unmatched neurons (
Adjustment of the auditory system in the dynamic auditory environment
Animal sounds are dynamic, changing values of multiple parameters which characterize them. So, one may consider that the changes evoked by repetitive focal electric stimulation or conditioning using repetitive tone burst stimulation may not occur in nature. The long-lasting stimulation has been used to evoke large, long-lasting changes for the clear-cut demonstration of plasticity and drug effects on the changes. Each of the electric pulses used for the bat research was 0.2 ms, 100 nA (e.g., Ma
Acknowledgments
This work was supported by a research grant from the National Institute on Deafness and Other Communication Disorders (DC-000175). I thank Ms. Sally E. Miller for editing this current manuscript and Dr. Philip H.S. Jen for his comments on it.
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