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The ascending and descending projections of the central auditory system form multiple tonotopic loops. This study specifically examines the tonotopic pathway from the auditory thalamus to the auditory cortex and then to the auditory midbrain in mice. We observed the changes of receptive fields in the central nucleus of the inferior colliculus of the midbrain evoked by focal electrical stimulation of the ventral division of the medial geniculate body of the thalamus. The receptive field of an auditory neuron was characterized by five parameters: the best frequency, minimum threshold, bandwidth, size of receptive field, and average spike number. We found that focal thalamic stimulation changed the parametric values characterizing the recorded collicular receptive fields toward those characterizing the stimulated thalamic receptive fields. Cortical inactivation with muscimol prevented the development of the collicular plasticity induced by focal thalamic stimulation. Our data suggest that the intact colliculo-thalamo-cortico-collicular loops are important for the coordination of sound-guided plasticity in the central auditory system.

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. In our present research with the awake big brown bat, we found that focal electric stimulation of collicular neurons evoked the BF shifts of collicular neurons located near the stimulated ones; that there were two types of BF shifts: centripetal and centrifugal BF shifts, i.e., shifts toward and shifts away from the BF of stimulated neurons, respectively; and that the development of these collicular BF shifts was blocked by inactivation of the auditory cortex. Our data indicate that the collicular BF shifts (plasticity) evoked by collicular electric stimulation depended on corticofugal feedback. It should be noted that collicular BF shifts also depend on acetylcholine because it has been demonstrated that atropine (an antagonist of muscarinic acetylcholine receptors) applied to the IC blocks the development of collicular BF shifts.

Plasticity of the auditory cortex can be induced by conditioning or focal cortical stimulation. The latter was used here to measure how stimulation in the tonotopy of the mouse primary auditory cortex influences frequency tuning in the midbrain central nucleus of the inferior colliculus (ICC). Shapes of collicular frequency tuning curves (FTCs) were quantified before and after cortical activation by measuring best frequencies, FTC bandwidths at various sound levels, level tolerance, Q-values, steepness of low- and high-frequency slopes, and asymmetries. We show here that all of these measures were significantly changed by focal cortical activation. The changes were dependent not only on the relationship of physiological properties between the stimulated cortical neurons and recorded collicular neurons but also on the tuning curve class of the collicular neuron. Cortical activation assimilated collicular FTC shapes; sharp and broad FTCs were changed to the shapes comparable to those of auditory nerve fibers. Plasticity in the ICC was organized in a center (excitatory)-surround (inhibitory) way with regard to the stimulated location (i.e., the frequency) of cortical tonotopy. This ensures, together with the spatial gradients of distribution of collicular FTC shapes, a sharp spectral filtering at the core of collicular frequency-band laminae and an increase in frequency selectivity at the periphery of the laminae. Mechanisms of FTC plasticity were suggested to comprise both corticofugal and local ICC components of excitatory and inhibitory modulation leading to a temporary change of the balance between excitation and inhibition in the ICC.