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

Abstract

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. The direction of contralateral BF shifts shows a flip-flop, depending on the spatial relationship between the stimulated and recorded neurons. This asymmetry in corticofugal modulation is mostly, if not totally, created by two subdivisions of the stimulated DSCF area that transmit signals to the contralateral DSCF area, presumably through the corpus callosum. This intriguing asymmetry in corticofugal modulation presumably functions for equalization of the reorganization of the frequency maps of the DSCF areas and subcortical auditory nuclei on both sides. auditory cortex ͉ cochlea ͉ inferior colliculus ͉ inhibition ͉ plasticity A long train of repetitive acoustic stimuli (1-4), repetitive electric stimulation of the primary auditory cortex (AC) (3-6), and auditory fear conditioning (7-9) each evoke plastic changes in frequency-tuning in both the AC and the central nucleus of the inferior colliculus (IC). The shift of a frequency-tuning curve is always accompanied by a best frequency (BF) shift. The collicular BF shift is the same for the conditioning and for cortical electric stimulation (3-4) and does not develop when the AC is inactivated during the conditioning (2, 8). Therefore, the collicular BF shift elicited by the conditioning is due to the corticofugal feedback. Atropine applied to the AC blocks the development of the cortical BF shift elicited by the conditioning but not the collicular BF shift. Therefore, the collicular BF shift does not depend on the cortical BF shift but on corticofugal feedback (9).The cortical and collicular BF shifts evoked by cortical electric stimulation are very similar to those elicited by auditory fear conditioning. A noticeable difference between them is that the cortical BF shift is long-term for the conditioning, but short-term for the electric stimulation (2,8,9). However, the cortical BF shift evoked by the electric stimulation changes from short-term to long-term when acetylcholine is applied to the AC (10). These observations indicate that focal cortical electric stimulation is an appropriate means for the exploration of the cortical and corticofugal function of the plasticity of the central auditory system in the normal adult animal.There are two types of BF shifts: centripetal and centrifugal. Centripetal BF ...

Bilateral Cortical Interaction: Modulation of Delay-Tuned Neurons in the Contralateral Auditory Cortex

“…Therefore, transcallosal inhibition must be mediated by GABAergic neurons activated by callosal fibers. Our current data and the data presented by Xiao and Suga (2005) indicate that bilateral cortical interactions consist of focused facilitation and widespread lateral inhibition. These interactions must be the most fundamental mechanisms for bilateral cortical interactions.…”

“…That is, DSCFd neurons show centripetal BF shifts to the contralateral DSCFd stimulation but centrifugal BF shifts to the contralateral DSCFv stimulation, whereas DSCFv neurons show centrifugal BF shifts to the contralateral DSCFd stimulation and centripetal BF shifts to the contralateral DSCFv stimulation (Xiao and Suga, 2005).…”

“…The effect of electric stimulation of the AC on the contralateral AC has been studied recently in the big brown bat (Ma and Suga, 2001) and the mustached bat (Xiao and Suga, 2005). In the big brown bat, contralateral BF shifts are centripetal and basically the same as ipsilateral BF shifts.…”

“…In the big brown bat, contralateral BF shifts are centripetal and basically the same as ipsilateral BF shifts. In the DSCF area of the mustached bat, unlike ipsilateral BF shifts, contralateral BF shifts are centripetal or centrifugal depending on the place where the electric stimulation is delivered (Xiao and Suga, 2005).…”

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

“…However, focal electric stimulation of the Doppler-shifted CF (DSCF) area (20) evokes centrifugal BF shifts of nearby BFunmatched DSCF neurons. The DSCF area is highly specialized for the fine analysis of biosonar signals in the frequency domain (21).…”