Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion

Abstract

In papers I and II of this series, we described two pairs of interneurons, Tr1 and Tr2, in the leech subesophageal ganglion which can trigger swimming activity in the isolated central nervous system (CNS). In this paper, we describe sensory inputs to these trigger neurons from previously identified mechanosensory neurons. We found that: Weak mechanical stimulation (stroking) of a body wall flap attached to a segmental ganglion in an otherwise isolated CNS excites the contralateral Tr1 slightly. Strong mechanical stimulation (pinching) of a mid-body wall flap evokes a burst of impulses in the contralateral Tr1. For both means of stimulation the effects on the ipsilateral Tr1 and on the Tr2 cell pair were much weaker. Stroking a body wall flap attached to the head ganglion (supra- and subesophageal ganglia) in an otherwise isolated CNS excites both Tr1s and both Tr2s, although the effect is weaker for the Tr2s. Pinching strongly excites both trigger neurons bilaterally. Pressure and nociceptive mechanosensory neurons (P and N cells) in the subesophageal ganglion and the first segmental ganglion appear to make direct excitatory synapses with the contralateral Tr1 and Tr2. Mechanosensory interactions with the ipsilateral trigger neurons appear to be indirect. Functional inactivation of Tr1 by hyperpolarization does not prevent swim initiation either by weak mechanical stimulation of a body-wall flap or by intracellular stimulation of P cells.2+ We conclude that the trigger neurons, Tr1 and Tr2, provide an excitatory pathway by which mechanosensory stimulation can initiate leech swimming activity.(ABSTRACT TRUNCATED AT 250 WORDS)

Physiological, pharmacological, and behavioral evidence for a TRPA1 channel that can elicit defensive responses in the medicinal leech

“…The initiation of swim behavior in the leech is quite complex, but one possibility is that swimming is elicited via direct activation of the P cells by AITC. Previous studies have found that both P and lN cell activity can produce swimming behavior, although P cells may be more effective (Brodfuehrer and Friesen, 1986;Debski and Friesen, 1987). At 500 µmol l −1 all of the animals produced a swim behavior, but there was a large variance in the duration of swimming elicited.…”

Dopamine Activates the Motor Pattern for Crawling in the Medicinal Leech

“…Swimming has been thoroughly described at the level of its patterngenerating neural networks (Brodfuehrer and Thorogood, 2001;Brodfuehrer et al, 1995a), gating cells (Kristan and Weeks, 1983), descending command-like cells (Brodfuehrer and Friesen, 1986;Brodfuehrer et al, 1995b;O'Gara and Friesen, 1995;Esch et al, 2002), and modulation by serotonin Crisp and Mesce, 2006). Insights into the neuronal bases of both these locomotor patterns can now be advanced by comparing their organization and regulation.…”

Statistics of Decision Making in the Leech

“…Moreover, recordings of the neural activity descending from the head ganglion in the connective have shown a massive coactivation of many unidentified interneurons during swimming episodes . Finally, direct stimulation of identified command neurons produces highly variable behavioral responses and often does not elicit any kind of behavior (Brodfuehrer and Friesen, 1986b). The same variability is encountered when strong mechanosensory stimuli are used to elicit swimming (Grobstein, 1994;.…”