Sensory function and gating of histaminergic neuron C2 in Aplysia

KR Weiss, HJ Chiel, I Kupfermann
1986 Journal of Neuroscience  
This paper explores the possible sensory function of the identified histaminergic neuron C2. Mechanical stimulation of a narrow region around the mouth of the animal (perioral zone) elicits brief depolarizing potentials in C2. Extracellular recordings from the peripheral axons of C2 indicate that the depolarizing potentials are due to action potentials that are conveyed from the periphery but do not invade the cell body, since they fail at a region with a low safety factor within the cerebral
more » ... thin the cerebral ganglion. These blocked axonal spikes (A-spikes) function as if they were excitatory synaptic inputs to C2, since the synaptic output of C2 does not occur unless the A-spikes succeed in evoking full action potentials in the soma (or an electrically close initial segment) of C2. Furthermore, like synaptic potentials, the A-spikes exhibit temporal and spatial summation, and facilitation. C2 receives both tonic and phasic inhibitory synaptic potentials, which can decrease the summation of A-spikes and thereby alter the frequency-filtering properties of C2 or block its synaptic output. Thus, C2 appears to be an unusual proprioceptive afferent that has a high degree of integrative function and may provide critical gating that is dependent on a variety of external and internal conditions. In previous work (Weiss et al., 1986a, b), we provided evidence that the identified histaminergic neuron C2 of Ap&ia fires during a feeding motor program and provides slow excitatory synaptic input to the metacerebral cell (MCC), a neuron that executes aspects of a food arousal state in the animal. The data suggest that C2 is an element of the circuits involved in mediating the food arousal state. During feeding motor programs, C2 exhibits depolarizing potentials that summate and drive the cell into a high-frequency burst of spikes. Although these depolarizing potentials are evoked by food stimuli, they are not directly dependent upon this chemosensory stimulation, since they continue to occur for a period of time after the chemosensory stimulation is terminated. In the present paper, we explore 2 questions: (1) what provides the excitatory potentials to C2, and (2) how might the activity of C2 be modulated? We provide evidence that C2 is a mechanoafferent neuron that can monitor some aspect of the feeding behavior of the animal. Furthermore, the synaptic output of C2 appears to be gated in an all-or-none fashion by inhibitory synaptic input and by electrotonically transmitted axon spikes that function like excitatory input to Neuroscience 0270-6474/86/0824 16-11%02.00/O the cells. Some of these results have appeared in a preliminary communication (Weiss et al., 1983) . Materials and Methods The electrophysiological methods used in this study were standard techniques, previously described. Intracellular recordings were obtained by means of double-barrel microelectrodes filled with 2 M potassium citrate. Three types ofpreparations were used: (1) semi-intact, (2) reduced, and (3) isolated nervous system. The semi-intact preparation (Weiss et al., 1986b) consisted of the isolated head in which the buccal artery was perfused with cooled seawater (15°C). The cerebral ganglion was pinned to a transilluminated stage and desheathed in order to expose C2 and the MCC. The reduced preparation consisted of the isolated cerebral ganglion, together with one or more lip nerves connected to the anterior tentacles, mouth, and jaws. In some experiments, an inflatable rubber "balloon" was inserted into the mouth in order to provide a reproducible mechanical stimulus to the jaws and perioral zone (Fig. 1) . The balloon was constructed of a thin-walled rubber finger cot, and was inflated by means of seawater injected through a polyethylene tube that was tied into the open end. In order to monitor the inflation of the balloon, pressure in the tube was measured by a Statham pressure gauge. Extracellular nerve recordings were made en passant by means of a doublemembrane electrode (Koch et al., 1984) or a polyethylene suction electrode into which a loop of nerve was drawn. The isolated preparation consisted of the cerebral ganglion connected only to the buccal ganglion, with all peripheral structures removed. Chemical synaptic transmission was blocked by a solution containing reduced Ca*+ concentration (0.5 x normal, 5 mM) and increased Mg2+ concentration (4 x normal, 200 mM). Results C2 is excited by mechanostimulation of the perioral zone We have previously found that in the isolated head preparation one could record excitatory potentials in C2 during one phase of the feeding motor program (Weiss et al., 1986b) . We showed that these excitatory potentials could be elicited by mechanical stimulation of the lip area, and that the amplitude of the potentials decreased as the cells were hyperpolarized. These observations were consistent with a hypothesis that the excitatory potentials were blocked axon spikes (A-spikes), and that cell C2 was an afferent neuron. In the first series of experiments designed to test this hypothesis, we attempted to determine if these excitatory potentials were due to central neurons that were excited during activation of central programs, or were associated with afferent input from the periphery. We eliminated all afferent input by using a preparation consisting of the isolated cerebral ganglion connected to the buccal ganglion. Rhythmic motor programs were elicited by stimulating the esophageal nerve at 1 Hz. In 10 preparations, such stimulation regularly evoked widespread activity in the buccal ganglion and in numerous cells in the E cluster of the cerebral ganglion. This activity probably reflected egestive, rather than ingestive, responses, but the esophageal nerve was used because, of all of the nerves, it evokes the most reliable and vigorous rhythmic output. Although C2 2416
doi:10.1523/jneurosci.06-08-02416.1986 pmid:3746415 fatcat:rjbb347zyrevbdidyk5wthcrrq