Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin‐A mRNA in Aplysia californica

Abstract

A previous study reported that a peptide, sensorin-A, is expressed exclusively in mechanosensory neurons having somata in central ganglia of Aplysia. The present study utilized in situ hybridization, staining by nerve back-fill and soma injection, and electrophysiological methods to characterize the locations, numbers, and functions of sensorin-A-expressing neurons and to define the relationships between soma locations and the locations of peripheral axons and receptive fields. Approximately 1,000 cells express sensorin-A mRNA in young adult animals (10-30 g) and 1,200 cells in larger adults (100-300 g). All of the labeled somata are in the CNS, primarily in the abdominal LE, rLE, RE and RF, pleural VC, cerebral J and K, and buccal S clusters. Expression also occurs in a few sparsely distributed cells in most ganglia. Together, receptive fields of all these mechanosensory clusters cover the entire body surface. Each VC cluster forms a somatotopic map of the ipsilateral body, a "sensory aplunculus." Cells in the pleural and cerebral clusters have partially overlapping sensory fields and synaptic targets. Buccal S cells have receptive fields on the buccal mass and lips and display notable differences in electrophysiological properties from other sensorin-A-expressing neurons. Neurons in all of the clusters have relatively high mechanosensory thresholds, responding preferentially to threatening or noxious stimuli. Synaptic outputs to target cells having defensive functions support a nociceptive role, as does peripheral sensitization following noxious stimulation, although additional functions are likely in some clusters. Interesting questions arise from observations that mRNA for sensorin-A is present not only in the somata but also in synaptic regions, connectives, and peripheral fibers.

Molecular Characterization of NMDA-Like Receptors inAplysiaandLymnaea:Relevance to Memory Mechanisms

“…The DIG-labeled antisense probes were hybridized to NR1 mRNA in whole-mount CNS preparations, and the neurons containing the probe-target duplex were localized and visualized with alkaline phosphatase-conjugated anti-DIG antibody fragments (Boehriger Mannheim). The detailed in situ hybridization protocol has been described Walters et al, 2004;Jezzini et al, 2005).…”

A Neuronal Isoform of Protein Kinase G Couples Mitogen-Activated Protein Kinase Nuclear Import to Axotomy-Induced Long-Term Hyperexcitability inAplysiaSensory Neurons

“…Answering this question has been extremely difficult using the complex mammalian nervous system. A experimentally favorable alternative is the homogeneous cluster of SNs that reside in the bilateral pleural ganglia of the mollusk Aplysia californica (Walters et al, 2004). Noxious mechanical stimulation of the body wall (Walters et al, 1983a) or crushing SN axons in vivo or in vitro, elicits an LTH with electrophysiological properties similar to those seen after axotomy of mammalian SNs (Walters et al, 1991;Walters, 1994;Bedi et al, 1998;Ungless et al, 2002;Sung and Ambron, 2004).…”

Localization of molecular correlates of memory consolidation to buccal ganglia mechanoafferent neurons after learning that food is inedible in Aplysia

“…1) have many features of morphology, physiology, and pharmacology in common with mechanoafferent neurons in the cerebral, pleural, and abdominal ganglia of Aplysia (Walters et al 2004). Pleural and abdominal ganglia mechanoafferent respond to stimulation of the skin, and connect to motor neurons and interneurons controlling withdrawal.…”

“…The buccal ganglia contain a central pattern generator (CPG) organizing repetitive consummatory feeding behaviors, as well as motor neurons innervating buccal muscles (Elliott and Susswein 2002), which move the toothed radula (Ye et al 2006;Neustadter et al 2007). The ganglia also contain primary mechanoafferents innervating the interior of the mouth (Evans and Cropper 1998;Walters et al 2004). Some of these mechanoafferents have properties similar to the mechanoafferents in abdominal and pleural ganglia that initiate withdrawal reflexes and that are a locus of long-term memory formation.…”

“…Sensorin-A is a peptide growth factor that is expressed exclusively in mechanoafferent neurons (Brunet et al 1991), including in some of the buccal ganglia mechanoafferents (Walters et al 2004). In other systems (Hu et al 2004(Hu et al , 2006Cai et al 2008), treatments causing long-term facilitation of mechanoafferent-to-motor-neuron synapses require increased expression of sensorin-A, which is released by the mechanoafferents and is sensed by them by binding to autocrine receptors.…”