Convergence of auditory-nerve fiber projections onto globular bushy cells

• Published in: Neuroscience 2005, Vol.136 (3), p.843-863
• Main Authors: Spirou, G.A., Rager, J., Manis, P.B.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; auditory; Auditory Pathways - anatomy & histology; Axons - ultrastructure; Biological and medical sciences; Brain Stem - cytology; Cats; Cell Count - methods; Cochlear Nerve - anatomy & histology; Cochlear Nerve - physiology; computational modeling; Ear and associated structures. Auditory pathways and centers. Hearing. Vocal organ. Phonation. Sound production. Echolocation; Electric Stimulation - methods; electron microscopy; endbulb; Fundamental and applied biological sciences. Psychology; Microscopy, Electron, Transmission - methods; Models, Anatomic; Models, Neurological; Nerve Endings - ultrastructure; Nerve Fibers - classification; Nerve Fibers - physiology; Nerve Net - cytology; Nerve Net - ultrastructure; Neural Inhibition - physiology; Neurons - cytology; Neurons - physiology; Neurons - ultrastructure; sound localization; synaptic integration; Time Factors; Vertebrates: nervous system and sense organs
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/j.neuroscience.2005.08.068

Globular bushy cells are a key element of brainstem circuits that mediate the early stages of sound localization. Many of their physiological properties have been attributed to convergence of inputs from the auditory nerve, many of which are large with complex geometry, but the number of these terminals contacting individual cells has not been measured directly. Herein we report, using cats as the experimental model, that this number ranged greatly (9–69) across a population of 12 cells, but over one-half of the cells (seven of 12) received between 15 and 23 inputs. In addition, we provide the first measurements of cell body surface area, which also varies considerably within this population and is uncorrelated with convergence. For one cell, we were able to document axonal structure over a distance greater than 100μm, between the soma and the location where the axon expanded to its characteristic large diameter. These data were combined with accumulated physiological information on vesicle release, receptor kinetics and voltage-gated ionic conductances, and incorporated into computational models for four cells that are representative of the structural variation within our sample population. This predictive model reveals that basic physiological features, such as precise first spike latencies and peristimulus time histogram shapes, including primary-like with notch and onset-L, can be generated in these cells without including inhibitory inputs. However, phase-locking is not significantly enhanced over auditory-nerve fibers. These combined anatomical and computational approaches reveal additional parameters, such as active zone density, nerve terminal size, numbers and sources of inhibitory inputs and their activity patterns, that must be determined and incorporated into next-generation models to understand the physiology of globular bushy cells.