Corticofugal regulation of auditory sensitivity in the bat inferior colliculus

Abstract

Under free-field stimulation conditions, corticofugal regulation of auditory sensitivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus, was studied by blocking activities of auditory cortical neurons with Lidocaine or by electrical stimulation in auditory cortical neuron recording sites. The corticocollicular pathway regulated the number of impulses, the auditory spatial response areas and the frequency-tuning curves of inferior colliculus neurons through facilitation or inhibition. Corticofugal regulation was most effective at low sound intensity and was dependent upon the time interval between acoustic and electrical stimuli. At optimal inter-stimulus intervals, inferior colliculus neurons had the smallest number of impulses and the longest response latency during corticofugal inhibition. The opposite effects were observed during corticofugal facilitation. Corticofugal inhibitory latency was longer than corticofugal facilitatory latency. Iontophoretic application of gamma-aminobutyric acid and bicuculline to inferior colliculus recording sites produced effects similar to what were observed during corticofugal inhibition and facilitation. We suggest that corticofugal regulation of central auditory sensitivity can provide an animal with a mechanism to regulate acoustic signal processing in the ascending auditory pathway.

Contribution of NMDA and AMPA Receptors to Temporal Patterning of Auditory Responses in the Inferior Colliculus

“…Neither factor accounts for longer first-spike latencies, up to 50 ms in IC (Parks and Pollak, 1993). Corticocollicular inputs could have longer latencies, and although some evidence suggests that cortical input can drive IC spikes (Syka and Popelar, 1984), most work suggests that cortical influence is modulatory (Jen et al, 1998;Suga et al, 2002). Other modulators of IC responses may alter first-spike latency [e.g., serotonin (Hurley and Pollak, 2005)] but are unlikely to both generate spikes from auditory input and delay the excitation.…”

Corticofugal modulation of directional sensitivity in the midbrain of the big brown bat, Eptesicus fuscus

“…As in our previous studies Jen et al, 1998Jen et al, , 2001Sun et al, 1996;Zhou and Jen, 2000a,b), one or two days before the recording session, a 1.8 cm nail was glued onto the exposed skull of each of 30 Nembutalanesthetized (45-50 mg/kg body weight) bats (body weight 17-25 g). Metofane and local anesthetic (Lidocaine) were used as supplements, when necessary, to minimize the pain and keep the animal in a quite and motionless state during the surgery.…”

“…During experiments, a pair of custom-made tungstenin-glass electrodes (tip: <10 m, inter-tip distance: 30-50 m, Jen et al, 1998;Sun et al, 1996) was used for recording acoustically evoked responses of AC neurons as well as for cortical electrical stimulation. As in our previous study , the electrodes were inserted into the AC at depths of 600-700 m (which is the Wfth layer of the AC where corticofugal Wbers originate, Games and Winer, 1988;Jen et al, 1997).…”

“…In our studies of corticofugal modulation of collicular signal processing, we have shown that cortical electrical stimulation decreases the number of impulses, sharpens the frequency tuning curve, compresses the rate-amplitude function, and decreases the auditory spatial response area of IC neurons (Sun et al, , 1996Jen et al, 1998Jen et al, , 2001Jen et al, , 2002Jen and Zhang, 1999;Zhou and Jen, 2000a,b). We have also shown that the eVect of corticofugal modulation is direction-dependent.…”

“…However, recent studies showed that the massive corticofugal system adjusts and improves subcortical multi-parametric auditory signal processing in bats, cats, guinea pigs, mice, and rats (Jen and Zhang, 1999;Jen et al, 1998Jen et al, , 2001Jen et al, , 2002He, 1997He, , 2003He et al, 2002;Ma and Suga, 2001a,b;Popelar et al, 2003;Suga et al, 1998Suga et al, , 2002Sun et al, 1989Sun et al, , 1996Syka and Popelar, 1984;Torterolo et al, 1998;Villa et al, 1991;Yan and Ehret, 2002;Yan and Suga, 1996;Zhou and Jen, 2000a,b). The corticofugal system also reorganizes (neuroplasticity) subcortical frequency map on the basis of sensory experience (including associative learning) Suga, 1998, 2000;Suga et al, 1997;Yan and Ehret, 2001;Yan and Suga, 1998;Zhang and Suga, 2000).…”