Interganglionic cerebral-buccal mechanoafferents of Aplysia: receptive fields and synaptic connections to different classes of neurons involved in feeding behavior.

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Abstract
A population of interganglionic mechanoafferent neurons (ICBM) capable of transmitting sensory information between the cerebral and buccal ganglia of Aplysia was identified and characterized. Their axon distributions, receptive-field properties, and synaptic connections indicate that they are involved in one or more aspects of feeding behavior. The ICBM somata (numbering 4-9 per hemiganglion) were visualized by cobalt backfills of a cerebral-buccal connective. Each ICBM neuron had 2 receptive fields: one relatively small receptive field confined to the perioral zone between the inner border of the lips and the chitinous jaws; and a 2nd, larger, buccal field located adjacent to the jaws along the anterior, inner wall of the buccal mass. These fields were innervated by axons passing in one or more cerebral and one or more buccal nerves, respectively. Field size, shape and mechanical sensitivity (within a field) varied. Sensory thresholds were relatively high and adjacent fields overlapped. ICBM neurons were normally silent but exhibited brisk, slowly adapting responses to punctate mechanical stimuli applied within their receptive fields. Intracellular stimulation of individual ICBM produced excitatory postsynaptic potentials (EPSP) in 3 classes of neurons: B cluster neurons and the metacerebral cells in the cerebral ganglion and multiaction neurons B4 and B5 in the buccal ganglion. All three types of excitatory follower cells appear to be related to one or another aspect of feeding behavior. Similar to other mechanoafferent neurons, the ICBM connections to B-cell neurons appear to be monosynaptic. The connections to the identified multiaction neurons B4 and B5 of the buccal ganglion are both monosynaptic and polysynaptic. Increasing the concentrations of divalent cations (Mg2+ and Ca2+) in the seawater bath to 3 times that of normal, thereby elevating the firing thresholds of central neurons, eliminated the later components of the EPSP, but the earliest components remained unchanged in amplitude and latency. Repeated low-frequency stimulation of ICBM neurons resulted in gradually decrementing EPSP responses. The compound EPSP evoked in B4 and B5 by firing of a single spike of an ICBM was relatively large (mean, 10.8 mV) and invariably evoked a postsynaptic spike or, occasionally, a train of spikes. Stimulation of ICBM neurons in bursts of 4 spikes evoked summating EPSP in B4 and B5, which could greatly outlast the period of stimulation. The summating EPSP exceeded spike threshold and frequently gave rise to an accelerating spike burst. Simultaneous extracellular recordings from buccal nerve 2 indicated that a pattern of buccal output involving at least six to eight neurons accompanied bursting activity in B4 and B5. Of ICBM tested 60% were monosynaptically coupled to the ipsilateral metacerebral cell (MCC). Collaterals of the same sensory neuron provide inputs both to neurons of a modulatory system as well as to specific motor neurons (B-cells and B4 and B5). The unitary EPSP amplitudes in the MCC were generally < 0.5 mV and were rarely sufficient to elicit a MCC spike. Mechanical stimulation of the perioral zone evoked compounds EPSP and sustained depolarizations capable of inducing repetitive MCC spiking.