Regulation of the segmental swim-generating system by a pair of identified interneurons in the leech head ganglion

Abstract

1. The aim of this study was to identify neurons that modulate activity of segmental swim gating interneurons. We found a pair of bilaterally symmetrical interneurons, cells SE1, whose activity level directly influences three groups of segmental neurons associated with generating swimming in the medicinal leech. 2. The somata of cells SE1 are located on the dorsal surface of the subesophageal ganglion. Their axons extend most, if not the entire, length of the ventral nerve cord and appear to make identical connections with the same group of swim-generating neurons in all segmental ganglia. 3. Cells SE1 excite monosynaptically all segmental swim gating interneurons, cells 204, examined. The level of excitation in cell 204 is directly correlated with the firing frequency of cell SE1. In most quiescent preparations (when the preparation is not swimming) hyperpolarization of a single cell SE1 eliminates all excitatory synaptic input to cells 204. 4. Cells SE1 excite monosynaptically three swim oscillatory interneurons, cells 115, 28, and 208. The strength of the connection from cell SE1 to cell 115 is stronger than the connection from cell SE1 to either cells 28 or 208. The level of excitation in cell 115 is directly correlated with the firing frequency of cell SE1. In most quiescent preparations, hyperpolarization of a single cell SE1 eliminates all excitatory synaptic input to cell 115 but has only a minor effect on the level of activity in cells 208 and 28. 5. Due most likely to the strong and direct connections cells SE1 have with swim gating and oscillatory interneurons, brief stimulation of cell SE1 can elicit swimming. Swimming generally occurs within 1 s after stimulation of cell SE1. During swimming, the membrane potential of cell SE1 depolarizes by 2-5 mV, and its firing frequency increases. Brief depolarization of cell SE1 during swimming reliably shifts the phase of the swimming rhythm, whereas longer periods of depolarization increase both swim period and burst duration. 6. Excitatory motor neurons to the dorsal longitudinal muscles, cells 3, 5, and 7, are strongly excited by stimulation of cell SE1. The firing frequency of cell 3 is positively correlated with the firing frequency of cell SE1. 7. The results of this study indicate that cells SE1 can modulate the level of excitation in three groups of neurons associated with generating leech swimming.(ABSTRACT TRUNCATED AT 400 WORDS)

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.…”

Discontinuous locomotion and prey sensing in the leech

“…The underlying mechanisms associated with this bias may involve neurons in the segmental and cephalic ganglia, which have been shown to promote crawling while inhibiting swimming (Brodfuehrer et al, 1995b;Esch et al, 2002;Briggman et al, 2005). Because dopamine plays a prominent role in promoting crawling while also suppressing swimming, prey detection most likely involves this amine (Crisp and Mesce, 2004;Crisp and Mesce, 2006;Puhl and Mesce, 2008).…”

Positive feedback loops sustain repeating bursts in neuronal circuits

“…Each also is continuously excited during fictive swimming; hence, each one is driven by the excitatory circuit. One cell 208 soma occurs in every midbody segment and many (perhaps all) receive excitatory synaptic input from the gating cells 204 and 205 [57] and from the cephalic swim excitor neuron cell SE1 [34]. Nevertheless, cell 208 does not directly feed excitation back onto these neurons; similarly, the gating neurons do not interact directly with each other.…”

“…Tactile stimulation of the body wall or depolarization of individual mechanosensory neurons activates swim-control neurons in the subesophageal ganglion, which include trigger neurons (Tr1 and Tr2) [30], the swim exciter neuron SE1 [34], and the R3b1 neuron [35]. Excitatory synapses connect Tr1 to swim-gating neurons cells 204/205 located in the posterior midbody ganglia (M9-M16) [36,37].…”

“…Cells 204 provide excitatory drive to a set of segmentally repeated swim oscillator interneurons (INs; cells 28, 115 and 208) via excitatory synapses [39]. Similarly, cell SE1 also directly excites swim-gating cells, oscillator cells, and swim-related MNs [34]. Because the swim-gating neurons (and SE1 cells) project to most, if not all, segmental ganglia, they provide massive excitation to activate the swim circuitry.…”