Identification of a New Neuropeptide Precursor Reveals a Novel Source of Extrinsic Modulation in the Feeding System of<i>Aplysia</i>

Proekt, Alex; Vilim, Ferdinand S.; Alexeeva, Vera; Březina, Vladimír; Friedman, Allyson K.; Jing, Jian; Li, Lingjun; Zhurov, Yuriy; Sweedler, Jonathan V.; Weiss, Klaudiusz R.

doi:10.1523/jneurosci.2932-05.2005

Cited by 39 publications

(42 citation statements)

References 65 publications

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“…Recent work indicates that the Aplysia feeding network is advantageous for studying central peptidergic modulation in the context of network multifunctionality Jing et al 2007;Koh and Weiss 2007;Koh et al 2003;Morgan et al 2002;Proekt et al 2005;Sasaki et al 2009;Sweedler et al 2002;Vilim et al 2010). In particular, these studies highlighted the essential roles of peptides in input neurons that are extrinsic to the CPG network.…”

Section: Roles Of Modulatory Peptides In Input Neurons: Comparisons Wmentioning

confidence: 99%

Composite Modulatory Feedforward Loop Contributes to the Establishment of a Network State

Vilim

Hatcher

et al. 2010

Journal of Neurophysiology

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Wu JS, Vilim FS, Hatcher NG, Due MR, Sweedler JV, Weiss KR, Jing J. Composite modulatory feedforward loop contributes to the establishment of a network state. J Neurophysiol 103: 2174-2184, 2010. First published February 24, 2010 doi:10.1152/jn.01054.2009 are one of many network motifs identified in a variety of complex networks, but their functional role in neural networks is not well understood. We provide evidence that combinatorial actions of multiple modulators may be organized as FFLs to promote a specific network state in the Aplysia feeding motor network. The Aplysia feeding central pattern generator (CPG) receives two distinct inputs-a higher-order interneuron cerebral-buccal interneuron-2 (CBI-2) and the esophageal nerve (EN)-that promote ingestive and egestive motor programs, respectively. EN stimulation elicits a persistent egestive network state, which enables the network to temporarily express egestive programs following a switch of input from the EN to CBI-2. Previous work showed that a modulatory CPG element, B65, is specifically activated by the EN and participates in establishing the egestive state by enhancing activity of egestion-promoting B20 interneurons while suppressing activity and synaptic outputs of ingestion-promoting B40 interneurons. Here a peptidergic contribution is mediated by small cardioactive peptide (SCP). Immunostaining and mass spectrometry show that SCP is present in the EN and is released on EN stimulation. Importantly, SCP directly enhances activity and synaptic outputs of B20 and suppresses activity and synaptic outputs of B40. Moreover, SCP promotes B65 activity. Thus the direct and indirect (through B65) pathways to B20 and B40 from SCPergic neurons constitute two FFLs with one functioning to promote egestive output and the other to suppress ingestive output. This composite FFL consisting of the two combined FFLs appears to be an effective means to co-regulate activity of two competing elements that do not inhibit each other, thereby contributing to establish specific network states.

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Section: Roles Of Modulatory Peptides In Input Neurons: Comparisons Wmentioning

confidence: 99%

Composite Modulatory Feedforward Loop Contributes to the Establishment of a Network State

Vilim

Hatcher

et al. 2010

Journal of Neurophysiology

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“…This indicates that network-generated responses are also determined by the network state at the time when a motor program is generated. States can be established by the presence of specific contextual stimuli (Nolen and Hoy, 1984;Hedwig, 2000;Esch et al, 2002) or hormones/modulator presence (HarrisWarrick and Marder, 1991;Morgan et al, 2000Morgan et al, , 2002Jing and Weiss, 2001;Wu et al, 2003;Proekt et al, 2005;Tryba et al, 2006;Koh and Weiss, 2007). In addition to being affected by the context, the network state is also affected by the history of its recent activity (Nadim et al, 1999;Proekt and Weiss, 2003;Proekt et al, 2004Proekt et al, , 2007.…”

Section: Phase Transition and Spike-onset Timingmentioning

confidence: 99%

State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network

Due²,

Sasaki³

et al. 2007

J. Neurosci.

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When sustained firing of a neuron is similar in different types of motor programs, its role in the generation of these programs is often similar. We investigated whether this is also the case for neurons involved in phase transition. In the Aplysia feeding central pattern generator (CPG), identified interneuron B64 starts firing at the transition between the protraction and the retraction phases of all types of motor programs, and its firing is sustained during the retraction phase. It was thought that B64 functions as a protraction terminator as it provides strong inhibitory input to protraction interneurons and motoneurons. Furthermore, premature activation of B64 can lead to premature termination of the protraction phase. Indeed, as we show here, B64 can terminate the protraction phase regardless of the type of motor program. However, B64 actually only functions as a protraction terminator in ingestive-like but not in egestive-like programs. This differential role of B64 results from a differential timing of the initiation of B64 spiking in the two types of programs. In turn, this differential timing of the initiation of B64 firing is determined by the internal state of the CPG. Thus, this study indicates the importance of the timing of initiation of firing in determining the functional role of a neuron and demonstrates that this role depends on the activity-dependent state of the network.

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“…B65 actions suggest that inputrepresenting neurons that are themselves elements of the CPG may play a role similar to that attributed to higher-order neurons. In addition, because B65 activity may be further regulated by other inputs, the mechanisms described in here may support additional forms of network and behavior flexibility Lum et al, 2005;Proekt et al, 2005;Zhurov et al, 2005;Jing et al, 2007).…”

Section: Discussionmentioning

confidence: 87%

An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network

Sasaki¹,

Jing²,

Due³

et al. 2008

J. Neurosci.

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Despite the importance of spike-timing regulation in network functioning, little is known about this regulation at the cellular level. In the Aplysia feeding network, we show that interneuron B65 regulates the timing of the spike initiation of phase-switch neurons B64 and cerebral-buccal interneuron-5/6 (CBI-5/6), and thereby determines the identity of the neuron that acts as a protraction terminator. Previous work showed that B64 begins to fire before the end of protraction phase and terminates protraction in CBI-2-elicited ingestive, but not in CBI-2-elicited egestive programs, thus indicating that the spike timing and phase-switching function of B64 depend on the type of the central pattern generator (CPG)-elicited response rather than on the input used to activate the CPG. Here, we find that CBI-5/6 is a protraction terminator in egestive programs elicited by the esophageal nerve (EN), but not by CBI-2, thus indicating that, in contrast to B64, the spike timing and protraction-terminating function of CBI-5/6 depends on the input to the CPG rather than the response type. Interestingly, B65 activity also depends on the input in that B65 is highly active in EN-elicited programs, but not in CBI-2-elicited programs independent of whether the programs are ingestive or egestive. Notably, during EN-elicited egestive programs, hyperpolarization of B65 delays the onset of CBI-5/6 firing, whereas in CBI-2-elicited ingestive programs, B65 stimulation simultaneously advances CBI-5/6 firing and delays B64 firing, thereby substituting CBI-5/6 for B64 as the protraction terminator. Thus, we identified a neural mechanism that, in an input-dependent manner, regulates spike timing and thereby the functional role of specific neurons.

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Identification of a New Neuropeptide Precursor Reveals a Novel Source of Extrinsic Modulation in the Feeding System ofAplysia

Cited by 39 publications

References 65 publications

Composite Modulatory Feedforward Loop Contributes to the Establishment of a Network State

Composite Modulatory Feedforward Loop Contributes to the Establishment of a Network State

State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network

An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network

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