Nucleus preeminentialis of mormyrid fish, a center for recurrent electrosensory feedback. I. Electrosensory and corollary discharge responses.
1. The nucleus preeminentialis (PE) is a large central structure that projects both directly and indirectly to the electrosensory lobe (ELL) where the primary afferents from electroreceptors terminate. PE receives electrosensory input directly from ELL and also from higher stages of the electrosensory pathway. PE is thus an important part of a central feedback loop that returns electrosensory information from higher stages of the system to the initial stage in ELL. 2. This study describes the field potentials and single-unit activity that are evoked in PE by electrosensory stimuli and by corollary discharge signals associated with the motor command that drives the electric organ to discharge. All recordings were extracellular in this study. 3. Two types of negative-going corollary discharge-evoked field potentials were found in PE: 1) a shallow, long-lasting negative wave with a latency at the peak of approximately 11 ms, and 2) a more sharply falling and larger negative wave with a shorter latency at the peak of approximately 9 ms. The long-latency wave was predominant in the dorsolateral and posterior parts of PE, whereas the short-latency wave was predominant in the medial and rostral regions. Both waves were only found in PE and thus can serve for its identification. 4. Electrosensory stimuli given either locally to a restricted skin region or symmetrically to the entire body evoked characteristic field potentials in both regions of PE. The mean latency between the stimulus and the peak of the response was 6.9 ms in the early negativity region and 12.2 ms in the late negative region. The responses to such stimuli were strongly facilitated by the electric organ corollary discharge. 5. Field potential responses to the electric organ corollary discharge were markedly plastic. Responses to the corollary discharge plus a paired electrosensory stimulus decreased over time and the response to the corollary discharge alone was markedly enhanced after a period of such pairing. 6. Local electrosensory stimulation of the skin showed that the caudal-rostral body axis is mapped from dorsal-medial to ventral-lateral in PE. The same somatotopy was found in the regions of the early and late negatives. The ventral and dorsal body appeared not to be separately mapped in PE. The areas representing the head and chin appendage ("Schnauzenorgan") are especially large in PE, due presumably to the high density of electroreceptors in these areas. 7. Two main types of units were recorded in PE: 1) inhibitory (I) cells with a corollary discharge response that was inhibited by an electrosensory stimulus to the center of their receptive fields; and 2) excitatory (E) cells with an excitatory response to electrosensory stimuli that was facilitated by the corollary discharge. Some of the E cells responded to the corollary discharge alone and some did not. Most cells appeared to be responding to input from mormyromast electroreceptors, but a few cells were driven by ampullary electroreceptors and a few by Knollenorgan electroreceptors. 8. The corollary discharge effects on I cells and E cells were plastic and depended on previous pairing with a sensory stimulus. The corollary discharge facilitation of E cells and inhibition of I cells decreased during pairing with a sensory stimulus, and the corollary discharge-driven excitation of I cells was much larger after pairing than before. 9. The results provide an initial overview of a major component in the control of electrosensory information processing by recurrent feedback from higher stages of the system.
Good Samaritan Hospital and Medical Center, R. S. Dow Neurological Sciences Institute, Portland, Oregon 97209-1595, USA.
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D000818:Animals; D001479:Basal Ganglia / Q000502:physiology*; D004557:Electric Organ / Q000502:physiology; D004594:Electrophysiology; D005246:Feedback / Q000502:physiology; D005260:Female; D005399:Fishes / Q000502:physiology*; D008297:Male; D008465:Mechanoreceptors / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology; D009046:Motor Neurons / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology; D012867:Skin / Q000294:innervation; D012879:Skin Physiological Phenomena; D013116:Spinal Cord / Q000166:cytology / Q000502:physiology