ABSTRACT
This research examines the mechanisms that initiate rhythmic activity in the episodic central pattern generator (CPG) underlying escape swimming in the gastropod mollusk Tritonia diomedea. Activation of the network is triggered by extrinsic excitatory input but also accompanied by intrinsic neuromodulation and the recruitment of additional excitation into the circuit. To examine how these factors influence circuit activation, a detailed simulation of the unmodulated CPG network was constructed from an extensive set of physiological measurements. In this model, extrinsic input alone is insufficient to initiate rhythmic activity, confirming that additional processes are involved in circuit activation. However, incorporating known neuromodulatory and polysynaptic effects into the model still failed to enable rhythmic activity, suggesting that additional circuit features are also required. To delineate the additional activation requirements, a large-scale parameter-space analysis was conducted (~2 x 10(6) configurations). The results suggest that initiation of the swim motor pattern requires substantial reconfiguration at multiple sites within the network, especially to recruit ventral swim interneuron-B (VSI) activity and increase coupling between the dorsal swim interneurons (DSIs) and cerebral neuron 2 (C2) coupling. Within the parameter space examined, we observed a tendency for rhythmic activity to be spontaneous and self-sustaining. This suggests that initiation of episodic rhythmic activity may involve temporarily restructuring a nonrhythmic network into a persistent oscillator. In particular, the time course of neuromodulatory effects may control both activation and termination of rhythmic bursting.
Subject(s)
Gastropoda/physiology , Neuronal Plasticity/physiology , Swimming/physiology , Tritonia Sea Slug/physiology , Action Potentials/physiology , Animals , Computer Simulation , Electric Stimulation , Electrophysiology , In Vitro Techniques , Membrane Potentials/physiology , Microelectrodes , Models, Neurological , Neural Networks, Computer , Neurons/classification , Neurons/physiology , Potassium Channels, Voltage-Gated/drug effects , Potassium Channels, Voltage-Gated/physiology , Reflex, Monosynaptic/physiology , Serotonin/physiology , Synapses/physiologyABSTRACT
Locomotion requires longitudinal co-ordination. We have examined uni-directional synaptic coupling processes between two classes of neuronal network oscillators: autonomously active "intrinsic" oscillators, and "potential" oscillators that lack sufficient excitatory drive for autonomous activity. We model such oscillator networks in the bilaterally-symmetrical, Xenopus tadpole spinal cord circuits that co-ordinate swimming. "Glutamate" coupling EPSPs can entrain a second oscillator of lower frequency provided their strength is sufficient. Fast (AMPA) EPSPs advance spiking on each cycle, while slow (NMDA) EPSPs increase frequency over many cycles. EPSPs can also enable rhythmicity in "potential" oscillators and entrain them. IPSPs operate primarily on a cycle-by-cycle basis. They can advance or delay spiking to entrain a second "intrinsic" oscillator with higher, equal or lower frequency. Bilaterally symmetrical coupling connections operate twice per cycle: once in each half-cycle, on each side of the receiving oscillator. Excitatory and inhibitory coupling allow entrainment in complimentary areas of parameter space.
Subject(s)
Chromosome Pairing/physiology , Models, Neurological , Neurons/physiology , Xenopus/physiology , Action Potentials , Animals , Biological Clocks , Computer Simulation , Interneurons/physiology , Locomotion/physiology , Motor Neurons/physiology , Neural Inhibition/physiology , Receptors, AMPA/physiology , Receptors, N-Methyl-D-Aspartate/physiology , Spinal Cord/physiology , Swimming/physiology , Time FactorsABSTRACT
The spiny projection neurons are by far the most numerous type of striatal neuron. In addition to being the principal projection neurons of the striatum, the spiny projection neurons also have an extensive network of local axon collaterals by which they make synaptic connections with other striatal projection neurons. However, up to now there has been no direct physiological evidence for functional inhibitory interactions between spiny projection neurons. Here we present new evidence that striatal projection neurons are interconnected by functional inhibitory synapses. To examine the physiological properties of unitary inhibitory postsynaptic potentials (IPSPs), dual intracellular recordings were made from pairs of spiny projection neurons in brain slices of adult rat striatum. Synaptic interactions were found in 9 of 45 pairs of neurons using averages of 200 traces that were triggered by a single presynaptic action potential. In all cases, synaptic interactions were unidirectional, and no bidirectional interactions were detected. Unitary IPSPs evoked by a single presynaptic action potential had a peak amplitude ranging from 157 to 319 microV in different connections (mean: 277 +/- 46 microV, n = 9). The percentage of failures of single action potentials to evoke a unitary IPSP was estimated and ranged from 9 to 63% (mean: 38 +/- 14%, n = 9). Unitary IPSPs were reversibly blocked by bicuculline (n = 4) and had a reversal potential of -62.4 +/- 0.7 mV (n = 5), consistent with GABA-mediated inhibition. The findings of the present study correlate very well with anatomical evidence for local synaptic connectivity between spiny projection neurons and suggest that lateral inhibition plays a significant role in the information processing operations of the striatum.
