Neural circuit flexibility in a small sensorimotor system

Abstract

Neuronal circuits underlying rhythmic behaviors (central pattern generators: CPGs) can generate rhythmic motor output without sensory input. However, sensory input is pivotal for generating behaviorally relevant CPG output. Here we discuss recent work in the decapod crustacean stomatogastric nervous system (STNS) identifying cellular and synaptic mechanisms whereby sensory inputs select particular motor outputs from CPG circuits. This includes several examples in which sensory neurons regulate the impact of descending projection neurons on CPG circuits. This level of analysis is possible in the STNS due to the relatively unique access to identified circuit, projection, and sensory neurons. These studies are also revealing additional degrees of freedom in sensorimotor integration that underlie the extensive flexibility intrinsic to rhythmic motor systems.

Figure 1

Identified sensory and projection neurons in the stomatogastric nervous system. (a) Soma location and partial projection pathways of identified projection neurons (MCN1, CPN2) and sensory neurons (AGR, VCN, PSR, GPR1/2) are indicated. All projection and sensory neurons shown, except AGR, are bilaterally symmetric. For details, see [29][••][61][87][88][89]. (b) Schematic illustration of the synaptic sites by which sensory inputs can select CPG output patterns, including via (1) actions onto CPG neurons, (2) actions onto projection neurons, and (3) presynaptic regulation of transmitter release from projection neurons onto CPG neurons. (c) The core CPG circuit diagram for the MCN1-driven gastric mill rhythm is shown. MCN1 uses its peptide cotransmitter CabTRP Ia to cause a slow excitation of the CPG neuron LG, and it uses GABA to cause a fast excitation of the CPG neuron Int1. LG inhibits transmitter release from the STG terminals of MCN1, without inhibiting its electrical coupling with MCN1. See references [84][90]. Symbols: filled circles, synaptic inhibition; t-bars, synaptic excitation; resistor, electrical coupling. Abbreviations: AGR: anterior gastric receptor; CabTRP Ia: Cancer borealis tachykinin-related peptide Ia; CoG: commissural ganglion; CPN2: commissural projection neuron 2; GABA: γ-amino butyric acid; GPR1/2: gastro-pyloric receptor 1/2; Int1: interneuron 1; LG: lateral gastric; MCN1: modulatory commissural neuron 1; Pro: protraction; PSR: posterior stomach receptors; Ret: retraction; STG: stomatogastric ganglion; VCN: ventral cardiac neuron.

Figure 2

Cotransmission and its modulation during sensorimotor integration in the crab STNS. (a) Tonic MCN1 stimulation drives the gastric mill rhythm, represented here by the regularly repeating bursting in the intracellular LG neuron recording. Top, During control conditions, GPR stimulation (during retraction phase: LG interburst) prolongs retraction, delaying the onset of the subsequent protraction phase (LG burst). Bottom, Bath applying the peptide hormone CCAP (10⁻⁷ M) weakens the GPR influence on the gastric mill rhythm. Adapted with permission from [••]. (b) GPR prolongs the gastric mill retractor phase by using its cotransmitter 5HT to presynaptically inhibit the projection neuron MCN1. This action decreases the MCN1 release of its peptide cotransmitter CabTRP Ia (represented by the thinner MCN1 axon) without altering its release of GABA, thereby selectively weakening MCN1 excitation of LG. The GPR synapses onto LG and Int1 (grey) are not effective during the MCN1-driven gastric mill rhythm. Adapted with permission from [••]. (c) The action of CCAP converges postsynaptically, in LG, with MCN1-released CabTRP Ia to activate the modulator-activated inward current (I_MI). This action enables CCAP to gate out the GPR action on the gastric mill rhythm by compensating for the decrease in CabTRP Ia-activated I_MI during the GPR presynaptic inhibition of MCN1. Adapted with permission from [••]. Symbols as in Figure 1.

Figure 3

Presynaptic regulation of parallel sensory feedback in the lobster STNS. (a) Moderate activity in the tendon organ receptor AGR excites the projection neurons CG and GI, with GI being less strongly activated than CG. The CG/GI co-activity elicits gastric mill motor pattern 1 (Pattern 1) from the gastric mill CPG in the STG. Pattern 1 is represented by the gastric mill motor neurons LG and GM generating co-active action potential bursts (filled black rectangles) that alternate with each LPG motor neuron burst. (b) Coactivating the muscle stretch-sensitive PSRs and AGR shifts the balance of projection neuron activity in favor of GI, via multiple mechanisms. First, the PSRs directly excite GI and inhibit CG. Second, they enhance GI activity by presynaptically strengthening AGR excitation of GI. Third, they reduce CG activity by presynaptically inhibiting the AGR excitation of CG. As a result, PSR/AGR coactivation drives a distinct gastric mill motor pattern (Pattern 2) in which LPG and GM bursts are coactive and alternate with each LG burst. Adapted with permission from [••].

Figure 4

Sensory and non-sensory functions of a tendon organ receptor in the crab STNS. (a) AGR has a peripheral spike initiation zone (SIZ), in or near its dendrites embedded in a gastric mill muscle, which generates phasic bursts of action potentials in response to rhythmic changes in muscle tension. AGR also has a central SIZ, located in the stomatogastric nerve (stn), which generates tonic spiking at a rate that is sensitive to locally applied octopamine [••]. (b) Schematic showing that small changes in the tonic AGR firing rate generated by its central SIZ alter the cycle period of an ongoing gastric mill motor pattern (LG bursting). Adapted with permission from [••]. (c) Schematic showing that phasic, higher frequency AGR spiking (mimicking its peripheral SIZ activation) entrains the gastric mill motor pattern (LG bursting). Adapted with permission from [61].