1. The Mauthner cell in fish and amphibians initiates an escape behaviour that has served as a model system for studies of the reticulospinal control of movement. This behaviour consists of a very rapid bend of the body and tail that is thought to arise from the monosynaptic excitation of large primary motoneurons by the Mauthner cell. Recent work suggests that the excitation fo primary motoneurons might be more complex than a solely monosynaptic connection. Toexamine this possibility, I used intracellular recording and staining to study the excitation of primary motoneurons by the M cell. 2. Simultaneous intracellular recordings from the M axon and ipsilateral primary motoneurons show that firing the M cell leads to complex postsynaptic potentials (PSPs) in the motoneurons. These PSPs usually have three components: and early, small, slow depolarization (component 1), a later, large, fast depolarization (component 2), and an even later, large, long-lasting depolarization (component 3). The first component has a latency of 0.52 +/- 0.15 (SD) ms, (n = 27) and most probably is a monosynaptic input from the M cell. This study focused on the two subsequent, less-understood parts of the PSP. Motoneurons typically fire off the second part of the PSP. This is usually (27 of 33 cells) the largest component, and it has a mean amplitude of 6.24 +/- 3.33 (SD) mV (n = 33) and a half-decay time of 0.44 +/- 0.18 (SD) ms (n = 27). The mean amplitude of the third component is 3.20 +/- 1.7 (SD) mV (n = 35), and its half-decay is 6.73 +/- 2.66 (SD) ms (n = 35). The latency of the second component averages 0.66 +/- 0.21 (SD) ms (n = 32), indicating that there are few synapses in the pathway mediating it. 3. One candidate pathway for the second component of the PSP involves a class of descending interneurons (DIs) that are monosynaptically, chemically excited by the M cell and appear in light microscopy to contact motoneurons. Simultaneous intracellular recordings from the M axon, a DI, and a primary motoneuron show that the interneurons are electronically coupled to monotoneurons and produce the fast, second component of the PSP. Direct excitation of an interneuron leads to a very short-latency (<0.2 ms), fast PSP in a motoneuron similar to the second component of the PSP produced by the M axon. The short latency and fatigue resistance of this connection indicate it is electrotonic, and this is supported by evidence for DC coupling between the two cells. Hyperpolarizing an interneuron to block its firing in response to excitation of the M cell reduces the second component of the PSP in a motoneuron, showing directly that the interneuron produces part of that component. 4. Several lines of evidence indicate that more than one DI terminates on each primary motoneuron. Direct activation of an interneuron produces only a fraction (12-84%) of the second component elicited by firing the M cell. Inflections on the second portion of the PSPs in motoneurons indicate that it may consist of several subcomponents, possibly arising from different cells. Hyperpolarization of an interneuron to remove it from the network reduces, but does not eliminate, the second part of the response in a motoneuron produced by firing the M cell. Lastly, increasing the firing rate of the M cell leads to discrete, large (26-74%) drops in the amplitude of the second component in a motoneuron, probably because of the loss of the input from interneurons as the chemical synapses at M axon/interneuron connections fatigue. Counts of inflections on the second components and peaks in amplitude histograms disclose that at least two to four interneurons converge on each motoneuron. The evidence indicates that the fast second component results from convergent input from relatively few powerful interneurons rather than a large pool of weak cells. 5. The second and third parts of PSPs are not obligatorily linked. Whereas both are always present at low stimulation frequencies, at higher frequencies, the third occurs iwthout the second and vice versa. The pathways mediating them are therefore at least partially independent of one another. The latency of the slow third component is 2-3 ms. This indicates that it arises via a polysynaptic pathway that most likely involves several synapses. The long latency establishes that it could not be produced by a disynaptic pathway involving input from DIs. This is consistent with the observation that these interneurons produce only coupling potentials in motoneurons. Thus the pathways mediating the second and third components are different, with the slow third part of the PSP arising from a polysynaptic pathway with more synapses than the pathway responsible for the second component. 6. Simultaneous recordings from an M axon and pairs of primary motoneurons reveal shared second components in motoneurons that most probably reflect divergence of individual DIs to more than one primary motoneuron. The pairwise recordings from motoneurons show no evidence of motoneuron/motoneuron coupling that might account for some parts of the PSPs produced by firing the M cell. 7. The presence and strength of the polysynaptic inputs to primary motoneurons require a revision of the standard view that primary motoneurons are driven solely by a monosynaptic input from the M axon. The motoneurons reach threshold via a combination of a depolarization of their initial segment by a direct input from the M axon (first component) and a larger, disynaptic, electrotonic iinput from DIs (second component). The polysynaptic pathways offer several new places for modifying the output of the network. They may play a role in the control of the trajectory of fish during escapes and provide an opportunity to understand better the way in which descending reticulospinal neurons interact with local spinal networks to produce an adaptive motor behavior.
