Chemoreception and mechanoreception in the gastropod molluscPleurobranchaea californica

Summary

Afferent chemosensory and mechanosensory pathways from peripheral sensory structures (the rhinophore and tentacle) to the cerebropleural ganglion (‘ brain ’) of the molluscPleurobranchaea were investigated using anatomical and electrophysiological methods. In both structures a sensory epithelium is connected by afferent nerves to a peripheral ganglion which sends a nerve (rhinophore or tentacle nerve) to the cerebropleural ganglion.

• 1. Filling the distal stumps of afferent nerves distal to the rhinophore and tentacle ganglia with cobaltous chloride (centrifugal fills of distal nerves) stained the somata of receptor cells in the sensory epithelium (Fig. 1), suggesting that primary afferent neurons project uninterrupted from the epithelium to the peripheral ganglia.

• 2. Filling proximal stumps of afferent nerves distal to the rhinophore and tentacle ganglia with cobaltous chloride (centripetal fills of distal nerves) stained mainly fiber tracts that terminated in the peripheral ganglia (Figs. 3, 5) suggesting that primary afferent input is processed mainly in these peripheral ganglia.

• 3. Filling distal stumps of nerves connecting the peripheral ganglia to the cerebropleural ganglion with cobaltous chloride (centrifugal fills of proximal nerves) stained approximately 100 somata in each peripheral ganglion but stained few axons in distal afferent nerves (Figs. 4, 5), suggesting that the rhinophore and tentacle nerves consist mainly of axons of interneurons arising in peripheral ganglia. Centripetal fills of proximal nerve stumps stained few (10–25) somata in the cerebropleural ganglion.

• 4. Transganglionic extracellular activity induced by extracellular stimulation of appropriate nerve roots was reversibly reduced in calcium-free sea water, indicating transmission of information across chemical synapses in the peripheral ganglia (Fig. 6).

• 5. Intracellular recordings were obtained from the somata of 79 interneurons in the tentacle and rhinophore ganglia while delivering sensory stimuli to the corresponding sensory structures. 53 cells showed reliably an action potential response to mechanical and/or chemical stimulation (Figs. 7, 9, 11–13, 15, 16, 18). The majority of cells were bimodal (mechano- and chemosensory), although monomodal (mechanosensory or chemosensory) cells were also encountered. In most cases (47/53) the response was excitatory, but in a few cases (6/53) inhibitory responses were obtained (Fig. 18).

• 6. Lucifer yellow injections were made for a representative number of such interneurons (Figs. 8, 10, 14, 17). Most of these showed monopolar neurons with a single axon passing from each soma into the rhinophore or tentacle nerve toward the cerebropleural ganglion, although injections of monomodal chemosensory interneurons (n = 2) revealed a bipolar configuration (Fig. 17).

• 7. The results collectively suggest that chemosensory and mechanosensory inputs from primary epithelial receptor cells of the rhinophore and tentacle are integrated in the peripheral ganglia and relayed to the central nervous system by a population of sensory interneurons.