Modulation of the excitability of cockroach giant interneurons during walking - II. Central and peripheral components

D. L. Daley, F. Delcomyn

Research output: Contribution to journalArticle

Abstract

1. There are two morphologically distinct groups of giant interneurons (GI's) in the American cockroach. The excitability of each of these groups is modulated during walking. The dorsal group of GI's (cells 5, 6, and 7) is excited while the ventral group of GI's (cells 1, 2, and 3) is inhibited. Here we show that there are both central and peripheral components to both the excitatory and inhibitory modulation. 2. Intracellular recordings were made from identified dorsal GI's (cells 5, 6, and 7) before and after severing the ventral nerve cord (VNC) anterior to the recording site. Severing the nerve cord greatly reduced the frequency of firing of all three dorsal GI's during walking (Fig. 1 and 2). Covering over the cerci (wind-sensitive abdominal appendages) with petroleum jelly further reduced the firing frequency of dorsal GI's during walking to the normal background level (compare Fig. 1 C and D). These results suggest that the major source of excitation of dorsal GI's during walking descends the VNC from thoracic or higher nervous centers. 3. Following deafferentation of thoracic and abdominal ganglia (only the paired cereal nerves and interganglionic connectives were left intact) intracellular recordings from identified dorsal GI's showed that these GI's were still excited during repetitive bursts of activity in leg motoneurons (Fig. 5) indicating that sensory input concomitant with walking was not the primary source of descending excitation. 4. The inhibitory modulation of ventral GI (cells 1, 2 and 3) excitability was investigated by comparing the sound responsiveness of individual ventral GI's to 50 Hz tone pulses in animals which were quiescent to that of the same ventral GI during bursts of motor activity in deafferented animals. Deafferentation experiments performed on ventral GI's 1, 2 and 3 all show that their sound responsiveness was reduced during bursts of leg motoneuron activity (Fig. 5). These results suggest that inhibitory modulation of the three large ventrally located GI's also has a central origin and is activated by the animal's walking. 5. Peripheral inhibitory modulation of ventral GI activity during walking was revealed in experiments performed on animals with ventral nerve cords cut anterior to the recording site. Intracellular recordings from these animals showed that the sound responsiveness of the three large ventral GI's (cells 1, 2 and 3) was still reduced during walking. These results suggest that during walking inhibitory modulation of ventral GI's originates from peripheral as well as central sources. 6. Sound responsiveness experiments with identified dorsal GI's showed that sensory input summates with descending excitation during walking to yield a greater number of spikes per tone pulse. When central descending pathways were cut, the increased sound responsiveness of dorsal GI's during walking was eliminated. Thus, when central descending input to dorsal GI's was eliminated, sound responsiveness was identical during resting and walking. 7. These results are discussed in relation to the organization and functional roles of the walking-associated modulation of GI excitability. It is argued that the central descending pathways dominate the observed modulation and that these pathways provide the most effective means of controlling GI excitability during walking.

Original languageEnglish (US)
Pages (from-to)241-251
Number of pages11
JournalJournal of Comparative Physiology □ A
Volume138
Issue number3
DOIs
StatePublished - Sep 1 1980

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ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Animal Science and Zoology
  • Behavioral Neuroscience

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