Roles of Inhibition in Complex Auditory Responses in the Inferior Colliculus: Inhibited Combination-Sensitive Neurons

• Published in: Journal of neurophysiology Vol. 95; no. 4; pp. 2179 - 2192
• Main Authors: Nataraj, Kiran, Wenstrup, Jeffrey J
• Format: Journal Article
• Language: English
• Published: United States Am Phys Soc 01-04-2006
• Subjects: Acoustic Stimulation; Action Potentials - drug effects; Action Potentials - physiology; Animals; Auditory Pathways - drug effects; Auditory Pathways - physiology; Bicuculline - pharmacology; Chiroptera; Electrophysiology; Evoked Potentials, Auditory, Brain Stem - drug effects; Evoked Potentials, Auditory, Brain Stem - physiology; GABA-A Receptor Antagonists; Inferior Colliculi - physiology; Neural Inhibition - drug effects; Neural Inhibition - physiology; Neurons, Afferent - drug effects; Neurons, Afferent - physiology; Receptors, GABA-A - physiology; Receptors, Glycine - antagonists & inhibitors; Receptors, Glycine - physiology; Strychnine - pharmacology
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.01148.2005

1 Department of Neurobiology, Northeastern Ohio Universities College of Medicine, Rootstown; and 2 Department of Biomedical Engineering, The University of Akron, Akron, Ohio
Submitted 31 October 2005;
accepted in final form 16 December 2005
We studied the functional properties and underlying neural mechanisms associated with inhibitory combination-sensitive neurons in the mustached bat's inferior colliculus (IC). In these neurons, the excitatory response to best frequency tones was suppressed by lower frequency signals (usually in the range of 12–30 kHz) in a time-dependant manner. Of 143 inhibitory units, the majority (71%) were type I, in which low-frequency sounds evoked inhibition only. In the remainder, however, the low-frequency inhibitory signal also evoked excitation. Of these, excitation preceded the inhibition in type E/I units (16%), whereas in type I/E units (13%), excitation followed the inhibition. Type E/I and I/E units were distinct in the tuning and threshold sensitivity of low-frequency responses, whereas type I units overlapped the other types in these features. In 71 neurons, antagonists to receptors for glycine [strychnine (STRY)] or GABA [bicuculline (BIC)] were applied microiontophoretically. These antagonists failed to eliminate combination-sensitive inhibition in 92% (STRY), 93% (BIC), and 87% (BIC + STRY) of the type I units tested. However, inhibition was reduced in many neurons. Results were similar for type E/I and I/E inhibitory neurons. The results indicate that there are distinct populations of combination-sensitive inhibited neurons in the IC and that these populations are at least partly independent of glycine or GABA A receptors in the IC. We propose that these populations originate in different brain stem auditory nuclei, that they may be modified by interactions within the IC, and that they may perform different spectrotemporal analyses of vocal signals.
Address for reprint requests and other correspondence: J. Wenstrup, Dept. of Neurobiology, Northeastern Ohio Universities College of Medicine, 4209 State Route 44, PO Box 95, Rootstown, OH 44272 (E-mail: jjw{at}neoucom.edu )