GABA-Induced Synaptic Facilitation at Type B to A Photoreceptor Connections in Hermissenda

Schultz, Laura M.; Clark, Gregory A.

doi:10.1016/s0361-9230(96)00325-5

Cited by 16 publications

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“…Using absolute real-time quantitative PCR (qPCR), we found that there was a strong correlation between the RSEM-predicted expression level in the transcriptome and the amount measured from whole-brain tissue by qPCR (Supplemental Fig. S4).GABA is another neurotransmitter that modulates light-movement paired learning (Schultz and Clark 1997;Blackwell 2002). No GABA receptor genes had been previously described from Hermissenda.…”

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confidence: 99%

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Identification of genes related to learning and memory in the brain transcriptome of the mollusc,Hermissenda crassicornis

2015

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The sea slug Hermissenda crassicornis (Mollusca, Gastropoda, Nudibranchia) has been studied extensively in associative learning paradigms. However, lack of genetic information previously hindered molecular-level investigations. Here, the Hermissenda brain transcriptome was sequenced and assembled de novo, producing 165,743 total transcripts. Orthologs of 95 genes implicated in learning were identified. These included genes for a serotonin receptor and a GABA-B receptor subunit that had not been previously described in molluscs, as well as an adenylyl cyclase gene not previously described in gastropods. This study illustrates the Hermissenda transcriptome's potential as an important genetic tool in future learning and memory research.[Supplemental material is available for this article.]Nervous systems of molluscs have been a focus of neuroscience research for many decades, yet their study has been impeded by lack of genetic information. The nudibranch Hermissenda crassicornis exhibits a simple form of associative learning, which has been studied extensively: it can learn to associate light changes with vestibular stimulation (Crow and Alkon 1978). The neural correlates of Hermissenda's associative memories formed during lightmovement pairings have been uncovered (Alkon 1980;Crow and Alkon 1980;Britton and Farley 1999;Tamse et al. 2003;Cavallo et al. 2014). Hermissenda has also been the subject of investigations related to many other aspects of neuroscience, including sensory and motor neuron physiology (Crow and Tian 2004;Nesse and Clark 2010;Jin and Crow 2011;Crow et al. 2013) and the evolution of behaviors and neurotransmitter systems Newcomb et al. 2012;Lillvis and Katz 2013). A limited number of molecular-level studies have been performed on Hermissenda in these areas (Nelson and Alkon 1988;Crow et al. 1997). Broader-scale genetic experiments, such as identification of genes or specific genetic isoforms that produce proteins involved in Hermissenda associative learning, have been impossible without more extensive genetic information specifically from Hermissenda.Transcriptomes have been sequenced in a small number of other gastropod species, including neuronal transcriptomes from Aplysia californica (Moroz et al. 2006;Fiedler et al. 2010;Heyland et al. 2011), A. kurodai (Lee et al. 2008Choi et al. 2010), Lymnaea stagnalis (Bouetard et al. 2012;Sadamoto et al. 2012), and Tritonia diomedea (Senatore et al. 2015), which have been used in studies of learning and other aspects of neuroscience. The field of molluscan neurogenomics is growing thanks in large part to recent advances in sequencing technologies, which allow larger amounts of transcriptomic information to be sequenced at lower costs compared with technologies available a few years ago.In this study, we describe the brain transcriptome of the sea slug Hermissenda crassicornis. The transcriptome was sequenced from central nervous system tissue mRNA, which included the cerebropleural ganglia, pedal ganglia, optic ganglia, eyes, and statocyst hair cells. S...

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confidence: 99%

“…GABA is another neurotransmitter that modulates light-movement paired learning (Schultz and Clark 1997;Blackwell 2002). No GABA receptor genes had been previously described from Hermissenda.…”

mentioning

confidence: 99%

Identification of genes related to learning and memory in the brain transcriptome of the mollusc,Hermissenda crassicornis

2015

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“…Type B photoreceptors suppress the behavior by inhibiting type A photoreceptors (Goh and Alkon, 1984). Furthermore, vestibular hair cells excite type B photoreceptors, thereby facilitating their inhibitory effect on type A photoreceptors (Schultz and Clark, 1997). Sensory information from photoreceptors and mechanoreceptors converges on type B cells to elicit phototactic behavior.…”

Section: Automodulation Of the Gain Of A Primary Sensory Organmentioning

confidence: 99%

“…Sensory information from photoreceptors and mechanoreceptors converges on type B cells to elicit phototactic behavior. Both GABA and serotonin act through the same biochemical pathway in these neurons (Schuman and Clark, 1994;Schultz and Clark, 1997). GABA, released by hair cells, binds to metabotropic receptors on the type B photoreceptors, stimulating phospholipase A2 to release arachidonic acid and thereby activate protein kinase C (PKC) (Muzzio et al, 2001).…”

Section: Automodulation Of the Gain Of A Primary Sensory Organmentioning

confidence: 99%

Neuromodulation in invertebrate sensory systems: from biophysics to behavior

Birmingham

Tauck²

2003

Journal of Experimental Biology

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SUMMARYNeuromodulation may enhance the ability of sensory circuits to respond appropriately to widely variable environmental stimuli. The functional significance of neuromodulation will emerge from understanding the effects of modulators not just on single cells and synapses, but also on networks and the behavior of intact animals. With their relatively simple circuitry and large identifiable cells, invertebrate nervous systems offer insights into the complex roles of neuromodulators in modifying networks to meet the changing needs of the animal. Here we describe the role of neuromodulation in several invertebrate sensory systems that have been studied at a variety of levels,from the biophysical up to the behavioral.

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“…In addition to the nonsynaptic enhancement in excitability detected after conditioning, enhancement of the amplitude of monosynaptic IPSPs has been observed in conditioned Hermissenda (Frysztak and Crow, 1994). Moreover, 5-HT and GABA, two putative neurotransmitters in the unconditioned stimulus (US) pathway, have been reported to produce enhancement of type B to type A photoreceptor synaptic connections (Schuman and Clark, 1994;Schultz and Clark, 1995). Secondmessenger pathways mediating the effects of 5-HT and GABA on enhanced excitability and synaptic enhancement have been studied recently (Matzel et al, 1990;Crow et al, 1991;Crow and Forrester, 1993;Yamoah and Crow, 1996).…”

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confidence: 99%

Synaptic Enhancement and Enhanced Excitability in Presynaptic and Postsynaptic Neurons in the Conditioned Stimulus Pathway ofHermissenda

Frysztak

Crow

1997

J. Neurosci.

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Identified type A photoreceptors of Hermissenda express differential effects of classical conditioning. Lateral type A photoreceptors exhibit an increase in excitability to both the conditioned stimulus (CS; light) and extrinsic current. In contrast, medial type A photoreceptors do not express enhanced excitability, but do show enhancement of the medial B to medial A synaptic connection. Therefore, both enhanced excitability and changes in synaptic strength may contribute to long-term plasticity underlying classical conditioning. The activation of protein kinase C (PKC) is involved in the induction of enhanced excitability of identified type B photoreceptors produced by one-trial conditioning and the expression of enhanced excitability in B photoreceptors after multitrial classical conditioning. We have examined a possible role for persistent kinase activity in the expression of enhanced excitability in lateral type A photoreceptors and enhancement of the medial B to medial type A synaptic connection after classical conditioning. Injection of the PKC inhibitor peptide PKC(19 -36) into medial type B photoreceptors of conditioned animals did not significantly change the amplitude of medial A IPSPs elicited by single spikes in the medial B photoreceptor. Injections of PKC(19 -36) into medial B photoreceptors of pseudorandom controls also did not significantly change the amplitude of IPSPs recorded from the medial A photoreceptor. In contrast, spikes elicited by extrinsic current in lateral type A photoreceptors of conditioned animals were significantly reduced in frequency after intracellular injection of PKC(19 -36) as compared with pseudorandom controls. Injection of the noninhibitory analog peptide [glu 27 ]PKC(19 -36) did not affect excitability. Thus, enhanced excitability in the lateral A photoreceptor of conditioned animals seems to be influenced, in part, by a constitutively active kinase or a persistent kinase activator, whereas synaptic enhancement of the connection between the medial B and medial A photoreceptors of conditioned animals may involve a different mechanism.

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GABA-Induced Synaptic Facilitation at Type B to A Photoreceptor Connections in Hermissenda

Cited by 16 publications

References 48 publications

Identification of genes related to learning and memory in the brain transcriptome of the mollusc,Hermissenda crassicornis

Identification of genes related to learning and memory in the brain transcriptome of the mollusc,Hermissenda crassicornis

Neuromodulation in invertebrate sensory systems: from biophysics to behavior

Synaptic Enhancement and Enhanced Excitability in Presynaptic and Postsynaptic Neurons in the Conditioned Stimulus Pathway ofHermissenda

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