Outputs of radula mechanoafferent neurons in Aplysia are modulated by motor neurons, interneurons, and sensory neurons.
The gain of sensory inputs into the nervous system can be modulated so that the nature and intensity of afferent input is variable. Sometimes the variability is a function of other sensory inputs or of the state of motor systems that generate behavior. A form of sensory modulation was investigated in the Aplysia feeding system at the level of a radula mechanoafferent neuron (B21) that provides chemical synaptic input to a group of motor neurons (B8a/b, B15) that control closure and retraction movements of the radula, a food grasping structure. B21 has been shown to receive both excitatory and inhibitory synaptic inputs from a variety of neuron types. The current study investigated the morphological basis of these heterosynaptic inputs, whether the inputs could serve to modulate the chemical synaptic outputs of B21, and whether the neurons producing the heterosynaptic inputs were periodically active during feeding motor programs that might modulate B21 outputs in a phase-specific manner. Four cell types making monosynaptic connections to B21 were found capable of heterosynaptically modulating the chemical synaptic output of B21 to motor neurons B8a and B15. These included the following: 1) other sensory neurons, e.g. , B22; 2) interneurons, e.g., B19; 3) motor neurons, e.g., B82; and 4) multifunction neurons that have sensory, motor, and interneuronal functions, e.g., B4/5. Each cell type was phasically active in one or more feeding motor programs driven by command-like interneurons, including an egestive motor program driven by CBI-1 and an ingestive motor program driven by CBI-2. Moreover, the phase of activity differed for each of the modulator cells. During the motor programs, shifts in B21 membrane potential were related to the activity patterns of some of the modulator cells. Inhibitory chemical synapses mediated the modulation produced by B4/5, whereas excitatory and/or electrical synapses were involved in the other instances. The data indicate that modulation is due to block of action potential invasion into synaptic release regions or to alterations of transmitter release as a function of the presynaptic membrane potential. The results indicate that just as the motor system of Aplysia can be modulated by intrinsic mechanisms that can enhance its efficiency, the properties of primary sensory cells can be modified by diverse inputs from mediating circuitry. Such modulation could serve to optimize sensory cells for the different roles they might play.
Rosen
S C
SC
Center for Neurobiology and Behavior, New York State Psychiatric Institute and College of Physicians and Surgeons of Columbia University, New York, New York 10032, USA.
Miller
M W
MW
Cropper
E C
EC
Kupfermann
I
I
D000818:Animals; D001048:Aplysia / Q000502:physiology*; D004558:Electric Stimulation; D004594:Electrophysiology; D005247:Feeding Behavior / Q000502:physiology; D017952:Ganglia, Invertebrate / Q000166:cytology / Q000502:physiology; D007395:Interneurons / Q000502:physiology* / Q000648:ultrastructure; D008465:Mechanoreceptors / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology; D009046:Motor Neurons / Q000502:physiology* / Q000648:ultrastructure; D009475:Neurons, Afferent / Q000502:physiology* / Q000648:ultrastructure; D015398:Signal Transduction / Q000502:physiology; D013268:Stimulation, Chemical