Plasticity of the adult auditory system based on corticocortical and corticofugal modulations.

Suga, N. Plasticity of the adult auditory system based on corticocortical and corticofugal modulations. NEUROSCI.

Inhibitory mechanisms shaping delay-tuned combination-sensitivity in the auditory cortex and thalamus of the mustached bat.

Delay-tuned auditory neurons of the mustached bat show facilitative responses to a combination of signal elements of a biosonar pulse-echo pair with a specific echo delay. The subcollicular nuclei produce latency-constant phasic on-responding neurons, and the inferior colliculus produces delay-tuned combination-sensitive neurons, designated "FM-FM" neurons. The combination-sensitivity is a facilitated response to the coincidence of the excitatory rebound following glycinergic inhibition to the pulse (1st harmonic) and the short-latency response to the echo (2nd-4th harmonics).

Specialization of the auditory system for the processing of bio-sonar information in the frequency domain: Mustached bats.

For echolocation, mustached bats emit velocity-sensitive orientation sounds (pulses) containing a constant-frequency component consisting of four harmonics (CF). They show unique behavior called Doppler-shift compensation for Doppler-shifted echoes and hunting behavior for frequency and amplitude modulated echoes from fluttering insects. Their peripheral auditory system is highly specialized for fine frequency analysis of CF (∼61.

Acuity in ranging based on delay-tuned combination-sensitive neurons in the auditory cortex of mustached bats.

A 1.0-ms echo delay from an emitted bio-sonar pulse at 25 °C corresponds to a 17.3-cm target distance.

Differences in velocity-information processing between two areas in the auditory cortex of mustached bats.

The bio-sonar pulse of the mustached bat, Pteronotus parnellii parnellii, consists of four harmonics of constant frequency (CF) and frequency-modulated (FM) components. The CF and FM components carry velocity and distance information, respectively. In the auditory cortex of mustached bats, the CC ("C" stands for constant frequency) and DIF (dorsal intrafossa) areas consist of CF/CF neurons tuned to a combination of pulse CF and echo CF (n = 2 or 3).

Synaptic mechanisms shaping delay-tuned combination-sensitivity in the auditory thalamus of mustached bats.

For the processing of target-distance information, delay-tuned auditory neurons of the mustached bat show facilitative responses to a combination of signal elements of a biosonar pulse-echo pair with a specific echo delay. They are initially produced in the inferior colliculus by facilitative responses based on the coincidence of the rebound response following glycinergic inhibition to the first harmonic of the pulse and a short-latency response to the 2nd-4th harmonics of its echo. Here, we report that further facilitative responses to pulse-echo pairs of thalamic delay-tuned neurons are mediated by glutamate receptors (NMDA and non-NMDA receptors), and that GABAergic inhibition shortens the duration of facilitative responses mediated by NMDA-receptors, without changing the delay tuning of thalamic delay-tuned neurons.

Neural processing of auditory signals in the time domain: delay-tuned coincidence detectors in the mustached bat.

The central auditory system produces combination-sensitive neurons tuned to a specific combination of multiple signal elements. Some of these neurons act as coincidence detectors with delay lines for the extraction of spectro-temporal information from sounds. "Delay-tuned" neurons of mustached bats are tuned to a combination of up to four signal elements with a specific delay between them and form a delay map.

Histaminergic modulation of nonspecific plasticity of the auditory system and differential gating.

In the auditory system of the big brown bat (Eptesicus fuscus), paired conditioned tonal (CS) and unconditioned leg stimuli (US) for auditory fear conditioning elicit tone-specific plasticity represented by best-frequency (BF) shifts that are augmented by acetylcholine, whereas unpaired CS and US for pseudoconditioning elicit a small BF shift and prominent nonspecific plasticity at the same time. The latter represents the nonspecific augmentations of auditory responses accompanied by the broadening of frequency tuning and decrease in threshold. It is unknown which neuromodulators are important in evoking the nonspecific plasticity.

Modulation of thalamic auditory neurons by the primary auditory cortex.

The central auditory system consists of the lemniscal and nonlemniscal pathways or systems, which are anatomically and physiologically different from each other. In the thalamus, the ventral division of the medial geniculate body (MGBv) belongs to the lemniscal system, whereas its medial (MGBm) and dorsal (MGBd) divisions belong to the nonlemniscal system. Lemniscal neurons are sharply frequency-tuned and provide highly frequency-specific information to the primary auditory cortex (AI), whereas nonlemniscal neurons are generally broadly frequency-tuned and project widely to cortical auditory areas including AI.

Tuning shifts of the auditory system by corticocortical and corticofugal projections and conditioning.

The central auditory system consists of the lemniscal and nonlemniscal systems. The thalamic lemniscal and nonlemniscal auditory nuclei are different from each other in response properties and neural connectivities. The cortical auditory areas receiving the projections from these thalamic nuclei interact with each other through corticocortical projections and project down to the subcortical auditory nuclei.

Corticocortical interactions between and within three cortical auditory areas specialized for time-domain signal processing.

In auditory cortex of the mustached bat, the FF (F means frequency modulation), dorsal fringe (DF), and ventral fringe (VF) areas consist of "combination-sensitive" neurons tuned to the pair of an emitted biosonar pulse and its echo with a specific delay (best delay: BD). The DF and VF areas are hierarchically at a higher level than the FF area. Focal electric stimulation of the FF area evokes "centrifugal" BD shifts of DF neurons, i.

Tone-specific and nonspecific plasticity of inferior colliculus elicited by pseudo-conditioning: role of acetylcholine and auditory and somatosensory cortices.

Experience-dependent plasticity in the central sensory systems depends on activation of both the sensory and neuromodulatory systems. Sensitization or nonspecific augmentation of central auditory neurons elicited by pseudo-conditioning with unpaired conditioning tonal (CS) and unconditioned electric leg (US) stimuli is quite different from tone-specific plasticity, called best frequency (BF) shifts, of the neurons elicited by auditory fear conditioning with paired CS and US. Therefore the neural circuits eliciting the nonspecific augmentation must be different from that eliciting the BF shifts.

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.

Tone-specific and nonspecific plasticity of the auditory cortex elicited by pseudoconditioning: role of acetylcholine receptors and the somatosensory cortex.

Experience-dependent plastic changes in the central sensory systems are due to activation of both the sensory and neuromodulatory systems. Nonspecific changes of cortical auditory neurons elicited by pseudoconditioning are quite different from tone-specific changes of the neurons elicited by auditory fear conditioning. Therefore the neural circuit evoking the nonspecific changes must also be different from that evoking the tone-specific changes.

Corticofugal modulation of the paradoxical latency shifts of inferior collicular neurons.

The central auditory system creates various types of neurons tuned to different acoustic parameters other than a specific frequency. The response latency of auditory neurons typically shortens with an increase in stimulus intensity. However, approximately 10% of collicular neurons of the little brown bat show a "paradoxical latency-shift (PLS)": long latencies to intense sounds but short latencies to weak sounds.

Modulation of auditory processing by cortico-cortical feed-forward and feedback projections.

The auditory center in the cerebrum, the auditory cortex, consists of multiple interconnected areas. The functional role of these interconnections is poorly understood. The auditory cortex of the mustached bat consists of at least nine areas, including the frequency modulation-frequency modulation (FF) and dorsal fringe (DF) areas.

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.

Bilateral cortical interaction: modulation of delay-tuned neurons in the contralateral auditory cortex.

Transcallosal excitation and inhibition have been theorized based on the effect of callosotomy on intractable epilepsy and dichotic listening research, respectively. We studied bilateral interaction of cortical auditory neurons and found that this interaction consisted of focused facilitation and widespread lateral inhibition. The frequency modulated (FM)-FM area of the auditory cortex of the mustached bat is composed of delay-tuned neurons tuned to the combination of the emitted biosonar pulse and its echo with a specific echo delay [best delay (BD)] and consists of three subdivisions in terms of the combination sensitivity of neurons.

Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning.

In the awake big brown bat, 30 min auditory fear conditioning elicits conditioned heart rate decrease and long-term best frequency (BF) shifts of cortical auditory neurons toward the frequency of the conditioned tone; 15 min conditioning elicits subthreshold cortical BF shifts that can be augmented by acetylcholine. The fear conditioning causes stress and an increase in the cortical serotonin (5-HT) level. Serotonergic neurons in the raphe nuclei associated with stress and fear project to the cerebral cortex and cholinergic basal forebrain.

Multiparametric corticofugal modulation of collicular duration-tuned neurons: modulation in the amplitude domain.

The subcortical auditory nuclei contain not only neurons tuned to a specific frequency but also those tuned to multiple parameters characterizing a sound. All these neurons are potentially subject to modulation by descending fibers from the auditory cortex (corticofugal modulation). In the past, we electrically stimulated cortical duration-tuned neurons of the big brown bat, Eptesicus fuscus, and found that its collicular duration-tuned neurons were corticofugally modulated in the frequency and time (duration) domains.

Asymmetry in corticofugal modulation of frequency-tuning in mustached bat auditory system.

Focal electric stimulation of the auditory cortex is well suited for exploration of the function of the corticofugal (descending) system and the neural mechanism of plasticity in the central auditory system, because it evokes changes in frequency-tuning, called best frequency (BF) shifts, as does auditory fear conditioning. The Doppler-shifted constant frequency (DSCF) area of the primary auditory cortex of the mustached bat is highly specialized for fine frequency analysis. Focal electric stimulation of the DSCF area evokes the BF shifts of ipsilateral cortical and collicular neurons away from the BF of stimulated neurons, whereas the stimulation evokes the BF shifts of contralateral cortical and collicular neurons either toward or away from the stimulated BF.

Effects of agonists and antagonists of NMDA and ACh receptors on plasticity of bat auditory system elicited by fear conditioning.

In big brown bats, tone-specific plastic changes [best frequency (BF) shifts] of cortical and collicular neurons can be evoked by auditory fear conditioning, repetitive acoustic stimuli or cortical electric stimulation. It has been shown that acetylcholine (ACh) plays an important role in evoking large long-term cortical BF shifts. However, the role of N-methyl-d-aspartate (NMDA) receptors in evoking BF shifts has not yet been studied.

Corticofugal feedback for collicular plasticity evoked by electric stimulation of the inferior colliculus.

Focal electric stimulation of the auditory cortex, 30-min repetitive acoustic stimulation, and auditory fear conditioning each evoke shifts of the frequency-tuning curves [hereafter, best frequency (BF) shifts] of cortical and collicular neurons. The short-term collicular BF shift is produced by the corticofugal system and primarily depends on the relationship in BF between a recorded collicular and a stimulated cortical neuron or between the BF of a recorded collicular neuron and the frequency of an acoustic stimulus. However, it has been unknown whether focal electric stimulation of the inferior colliculus evokes the collicular BF shift and whether the collicular BF shift, if evoked, depends on corticofugal feedback.

Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex.

Auditory fear conditioning with tone bursts followed by electric leg stimulation activates neurons not only in the auditory and somatosensory systems but also in many other regions of the brain and elicits shifts in the best frequencies (BFs) of collicular and cortical neurons, i.e., reorganization of the frequency (co-chleotopic) maps in the inferior colliculus and auditory cortex (AC).