Submicrosecond Pacemaker Precision is Behaviorally Modulated: The Gymnotiform Electromotor Pathway

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 95; no. 8; pp. 4684 - 4689
• Main Authors: Moortgat, Katherine T., Keller, Clifford H., Bullock, Theodore H., Sejnowski, Terrence J.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences of the United States of America 14.04.1998; National Acad Sciences; National Academy of Sciences; The National Academy of Sciences
• Subjects: Activity Cycles; Animal behavior; Animal Communication; Animal vocalization; Animals; Behavioral neuroscience; Biological Sciences; Electric Fish; Electric Organ - physiology; Electrophysiology - methods; Female; Fish; Frequency ranges; Histograms; Lesions; Light; Male; Mental stimulation; Minimum value; Neurobiology; Neurology; Neurons; Neurons - physiology; Oscillometry; Sensitivity and Specificity; Species Specificity
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.95.8.4684

What are the limits and modulators of neural precision? We address this question in the most regular biological oscillator known, the electric organ command nucleus in the brainstem of wave-type gymnotiform fish. These fish produce an oscillating electric field, the electric organ discharge (EOD), used in electrolocation and communication. We show here that the EOD precision, measured by the coefficient of variation (CV = SD/mean period) is as low as 2 × 10-4in five species representing three families that range widely in species and individual mean EOD frequencies (70-1,250 Hz). Intracellular recording in the pacemaker nucleus (Pn), which commands the EOD cycle by cycle, revealed that individual Pn neurons of the same species also display an extremely low CV (CV = 6 × 10-4, 0.8 μ s SD). Although the EOD CV can remain at its minimum for hours, it varies with novel environmental conditions, during communication, and spontaneously. Spontaneous changes occur as abrupt steps (250 ms), oscillations (3-5 Hz), or slow ramps (10-30 s). Several findings suggest that these changes are under active control and depend on behavioral state: mean EOD frequency and CV can change independently; CV often decreases in response to behavioral stimuli; and lesions of one of the two inputs to the Pn had more influence on CV than lesions of the other input.