Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer at Aplysia Sensorimotor Synapses: Empirical and Computational Analyses
The Aplysia sensorimotor synapse is a key site of plasticity for several simple forms of learning. Plasticity of this synapse has been extensively studied, albeit primarily with individual action potentials elicited at low frequencies. Yet, the mechanosensory neurons fire high-frequency bursts in re...
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Veröffentlicht in: | The Journal of neuroscience 2003-09, Vol.23 (23), p.8392-8401 |
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description | The Aplysia sensorimotor synapse is a key site of plasticity for several simple forms of learning. Plasticity of this synapse has been extensively studied, albeit primarily with individual action potentials elicited at low frequencies. Yet, the mechanosensory neurons fire high-frequency bursts in response to even moderate tactile stimuli delivered to the skin. In the present study, we extend this analysis to show that sensory neurons also fire bursts in the range of 1-60 Hz in response to electrical stimuli similar to those used in behavioral studies of sensitization. Intracellular stimulation of sensory neurons to fire a burst of action potentials at 10 Hz for 1 sec led to significant homosynaptic depression of postsynaptic responses. The depression was transient and fully recovered within 10 min. During the burst, the steady-state depressed phase of the postsynaptic response, which was only 20% of the initial EPSP of the burst, still contributed to firing the motor neuron. To explore the functional contribution of transient homosynaptic depression to the response of the motor neuron, computer simulations of the sensorimotor synapse with and without depression were compared. Depression allowed the motor neuron to produce graded responses over a wide range of presynaptic input strength. In addition, enhancement of synaptic transmission throughout a burst increased motor neuron output substantially more than did preferential enhancement of the initial phase of a burst. Thus, synaptic depression increased the dynamic range of the sensorimotor synapse and can, in principle, have a profound effect on information processing. |
doi_str_mv | 10.1523/jneurosci.23-23-08392.2003 |
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To explore the functional contribution of transient homosynaptic depression to the response of the motor neuron, computer simulations of the sensorimotor synapse with and without depression were compared. Depression allowed the motor neuron to produce graded responses over a wide range of presynaptic input strength. In addition, enhancement of synaptic transmission throughout a burst increased motor neuron output substantially more than did preferential enhancement of the initial phase of a burst. 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Plasticity of this synapse has been extensively studied, albeit primarily with individual action potentials elicited at low frequencies. Yet, the mechanosensory neurons fire high-frequency bursts in response to even moderate tactile stimuli delivered to the skin. In the present study, we extend this analysis to show that sensory neurons also fire bursts in the range of 1-60 Hz in response to electrical stimuli similar to those used in behavioral studies of sensitization. Intracellular stimulation of sensory neurons to fire a burst of action potentials at 10 Hz for 1 sec led to significant homosynaptic depression of postsynaptic responses. The depression was transient and fully recovered within 10 min. During the burst, the steady-state depressed phase of the postsynaptic response, which was only 20% of the initial EPSP of the burst, still contributed to firing the motor neuron. To explore the functional contribution of transient homosynaptic depression to the response of the motor neuron, computer simulations of the sensorimotor synapse with and without depression were compared. Depression allowed the motor neuron to produce graded responses over a wide range of presynaptic input strength. In addition, enhancement of synaptic transmission throughout a burst increased motor neuron output substantially more than did preferential enhancement of the initial phase of a burst. Thus, synaptic depression increased the dynamic range of the sensorimotor synapse and can, in principle, have a profound effect on information processing.</description><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Aplysia</subject><subject>Aplysia - physiology</subject><subject>Behavioral/Systems/Cognitive</subject><subject>Computer Simulation</subject><subject>Electric Stimulation</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Long-Term Synaptic Depression - physiology</subject><subject>Models, Neurological</subject><subject>Motor Neurons - physiology</subject><subject>Neural Inhibition - physiology</subject><subject>Neural Networks (Computer)</subject><subject>Neurons, Afferent - physiology</subject><subject>Synapses - physiology</subject><subject>Synaptic Transmission - physiology</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkttu1DAQhi0EotvCKyCLC7jK4kMOTi-QlrBAUKES215bjuN0XSV2ajus9mX6rHg3Kw5XSJYtz3zzz4w9ALzGaIkzQt_dGzU566VeEprEhRgtyZIgRJ-ARSTKhKQIPwULRAqU5GmRnoFz7-8RQgXCxXNwhkmZM4TwAjx-mJwPSW3aSaoWbvZGjEFL-FGNTnmvrYHCtLAOHn6z7dSLcDBV1gSnmykoGCysTWfdMHtunDC-Uw6KAFdjv_dawI0y3jo92GDdnMErfwnXw6idlqI_ZqjsME7hKBItq7jtI_UCPOtE79XL03kBbj-tb6ovydX157paXSUypTQkAqlMINqxTOAU5wyzUmWKFSojkiBRZF1Dyi5vS4Zz2hSx-eguWcnaXDYyJ_QCvJ91x6kZVCtV7E_0fIxVC7fnVmj-r8foLb-zP3lepPFRiyjw5iTg7MOkfOCD9lL1vTDKTp4XNMdpych_wVh6hlKSR_ByBmX8a-9U97sajPhhDvjX7-vbH9ebqubxEtdxDvhhDmLwq7_7-RN6-vgIvJ2Brb7b7rRT3A-i7yOO-W63mwUPevQXvtLDXQ</recordid><startdate>20030910</startdate><enddate>20030910</enddate><creator>Phares, Gregg A</creator><creator>Antzoulatos, Evangelos G</creator><creator>Baxter, Douglas A</creator><creator>Byrne, John H</creator><general>Soc Neuroscience</general><general>Society for Neuroscience</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20030910</creationdate><title>Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer at Aplysia Sensorimotor Synapses: Empirical and Computational Analyses</title><author>Phares, Gregg A ; Antzoulatos, Evangelos G ; Baxter, Douglas A ; Byrne, John H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c433t-a0e5a03f85a14168189e5e87e52c20a75fb29f6d98163b7968e5e9898d6cbc623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Aplysia</topic><topic>Aplysia - physiology</topic><topic>Behavioral/Systems/Cognitive</topic><topic>Computer Simulation</topic><topic>Electric Stimulation</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>Long-Term Synaptic Depression - physiology</topic><topic>Models, Neurological</topic><topic>Motor Neurons - physiology</topic><topic>Neural Inhibition - physiology</topic><topic>Neural Networks (Computer)</topic><topic>Neurons, Afferent - physiology</topic><topic>Synapses - physiology</topic><topic>Synaptic Transmission - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Phares, Gregg A</creatorcontrib><creatorcontrib>Antzoulatos, Evangelos G</creatorcontrib><creatorcontrib>Baxter, Douglas A</creatorcontrib><creatorcontrib>Byrne, John H</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Phares, Gregg A</au><au>Antzoulatos, Evangelos G</au><au>Baxter, Douglas A</au><au>Byrne, John H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer at Aplysia Sensorimotor Synapses: Empirical and Computational Analyses</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2003-09-10</date><risdate>2003</risdate><volume>23</volume><issue>23</issue><spage>8392</spage><epage>8401</epage><pages>8392-8401</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>The Aplysia sensorimotor synapse is a key site of plasticity for several simple forms of learning. 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To explore the functional contribution of transient homosynaptic depression to the response of the motor neuron, computer simulations of the sensorimotor synapse with and without depression were compared. Depression allowed the motor neuron to produce graded responses over a wide range of presynaptic input strength. In addition, enhancement of synaptic transmission throughout a burst increased motor neuron output substantially more than did preferential enhancement of the initial phase of a burst. Thus, synaptic depression increased the dynamic range of the sensorimotor synapse and can, in principle, have a profound effect on information processing.</abstract><cop>United States</cop><pub>Soc Neuroscience</pub><pmid>12968001</pmid><doi>10.1523/jneurosci.23-23-08392.2003</doi><tpages>10</tpages></addata></record> |
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subjects | Action Potentials - physiology Animals Aplysia Aplysia - physiology Behavioral/Systems/Cognitive Computer Simulation Electric Stimulation Excitatory Postsynaptic Potentials - physiology Long-Term Synaptic Depression - physiology Models, Neurological Motor Neurons - physiology Neural Inhibition - physiology Neural Networks (Computer) Neurons, Afferent - physiology Synapses - physiology Synaptic Transmission - physiology |
title | Burst-Induced Synaptic Depression and Its Modulation Contribute to Information Transfer at Aplysia Sensorimotor Synapses: Empirical and Computational Analyses |
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