The Neuronal Basis of the Behavioral Choice between Swimming and Shortening in the Leech: Control Is Not Selectively Exercised at Higher Circuit Levels

Abstract

Swimming and the whole-body shortening reflex are two incompatible behaviors performed by the medicinal leech Hirudo medicinalis. We set out to examine the neuronal basis of the choice between these behaviors, taking advantage of the fact that the neuronal circuit underlying swimming is relatively well understood. The leech swim circuit is organized hierarchically and contains three interneuronal levels, including two upper levels of "command-like" neurons. We tested the responses of the swim circuit neurons to stimuli that produced shortening, using reduced preparations in which neurophysiological recording could be performed while behaviors were elicited. We found that the majority of the swim circuit neurons, including most of the command-like cells and all of the cells at the highest hierarchical level of the circuit, were excited by stimuli that produced shortening as well as by stimuli that produced swimming. Only a subset of neurons, at levels below the top, were inhibited during shortening; these included one of the command-like cells and an oscillator cell (an interneuron that is part of the central pattern generator for swimming). These results imply that the control of the choice between swimming and shortening is not exercised selectively at the higher levels of the swim circuit.

Statistics of Decision Making in the Leech

“…Neurons Tr1, SE1, and R3b1 initiate swimming (Brodfuehrer and Friesen, 1986a,b,c;Thorogood and Brodfuehrer 1995;Shaw and Kristan, 1997;Esch et al, 2002), whereas neurons SIN1 and Tr2 terminate swimming O'Gara and Friesen, 1995). The firing of neuron R3b1 (Esch et al, 2002) elicits both swimming and crawling or a hybrid behavior (similar to that shown in Fig.…”

“…An automatic system based on imaging with a CCD camera tracked three colored beads attached to the back of the leech and recorded its motion for up to 12 h. Statistical analysis based on the kinematic and spectral content of the leech motion (Mazzoni et al, 2005) allowed unambiguous classification of Ͼ90% of the leech motion into characteristic behavioral categories. We found that the mechanism by which the leech decides its behavior is adequately described by a Markov process, the transition rates of which are probably controlled by the firing of command-like neurons found in the leech head ganglion O'Gara and Friesen, 1995;Shaw and Kristan, 1997;Esch et al, 2002).…”

“…7), depending on the sensory environment (the depth of the fluid surrounding the leech); however, leech behavioral decisions are likely to depend on a much more distributed neural dynamics than just the activity of this set of neurons. In fact, behavioral choice experiments have shown that most of these neurons are multifunctional, i.e., they are activated during different behaviors such as swimming and whole-body shortening (Tr1 and SE1) (Shaw and Kristan, 1997) or swimming and crawling (R3b1) (Esch et al, 2002). 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 .…”

Responses to Conflicting Stimuli in a Simple Stimulus–Response Pathway

“…Such an outcome could be considered in the context of behavioral choice (e.g., Shaw and Kristan, 1997;Briggman et al, 2005;Körding and Wolpert, 2006).…”

Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

“…This coding scheme has received the most attention in studies involving a directed response (Georgopoulos et al, 1986;Sparks, 1988;Georgopoulos, 1995;Lewis and Kristan, 1998a,b;Lewis, 1999), but it can be extended to include categorically distinct behaviors . A recent hypothesis proposes that different motor behaviors result from different combinations of activity patterns in overlapping but distinct combinations of multifunctional neuronal inputs to motor circuits Shaw and Kristan, 1997). With respect to sensory-evoked activation of the descending reticulospinal neuron system that activates the spinal locomotor network or the VCN-evoked activation of projection neurons that activate the gastric mill circuit, the resulting network and behavioral output also result from activity that is represented across a population of descending inputs.…”