Differential Modulation of Synaptic Strength and Timing Regulate Synaptic Efficacy in a Motor Network

被引:19
作者
Johnson, Bruce R. [1 ]
Brown, Jessica M. [1 ]
Kvarta, Mark D. [1 ]
Lu, Jay Y. J. [1 ]
Schneider, Lauren R. [1 ]
Nadim, Farzan [2 ,3 ]
Harris-Warrick, Ronald M. [1 ]
机构
[1] Cornell Univ, Dept Neurobiol & Behav, Ithaca, NY 14853 USA
[2] Rutgers State Univ, Dept Biol Sci, Newark, NJ 07102 USA
[3] Rutgers State Univ, New Jersey Inst Technol, Dept Math Sci, Newark, NJ 07102 USA
基金
美国国家卫生研究院;
关键词
LOBSTER STOMATOGASTRIC GANGLION; UNDERLYING PATTERN GENERATION; TRANSIENT POTASSIUM CURRENT; DOPAMINE MODULATION; AMINE MODULATION; SELECTIVE INACTIVATION; IDENTIFIED NEURONS; PYLORIC NETWORK; PHASE-SHIFTS; MECHANISMS;
D O I
10.1152/jn.00809.2010
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Johnson BR, Brown JM, Kvarta MD, Lu JYJ, Schneider LR, Nadim F, Harris-Warrick RM. Differential modulation of synaptic strength and timing regulate synaptic efficacy in a motor network. J Neurophysiol 105: 293-304, 2011. First published November 3, 2010; doi:10.1152/jn.00809.2010. Neuromodulators modify network output by altering neuronal firing properties and synaptic strength at multiple sites; however, the functional importance of each site is often unclear. We determined the importance of monoamine modulation of a single synapse for regulation of network cycle frequency in the oscillatory pyloric network of the lobster. The pacemaker kernel of the pyloric network receives only one chemical synaptic feedback, an inhibitory synapse from the lateral pyloric (LP) neuron to the pyloric dilator (PD) neurons, which can limit cycle frequency. We measured the effects of dopamine (DA), octopamine (Oct), and serotonin (5HT) on the strength of the LP -> PD synapse and the ability of the modified synapse to regulate pyloric cycle frequency. DA and Oct strengthened, whereas 5HT weakened, LP -> PD inhibition. Surprisingly, the DA-strengthened LP -> PD synapse lost its ability to slow the pyloric oscillations, whereas the 5HT-weakened LP -> PD synapse gained a greater influence on the oscillations. These results are explained by monoamine modulation of factors that determine the firing phase of the LP neuron in each cycle. DA acts via multiple mechanisms to phase-advance the LP neuron into the pacemaker's refractory period, where the strengthened synapse has little effect. In contrast, 5HT phase-delays LP activity into a region of greater pacemaker sensitivity to LP synaptic input. Only Oct enhanced LP regulation of cycle period simply by enhancing LP -> PD synaptic strength. These results show that modulation of the strength and timing of a synaptic input can differentially affect the synapse's efficacy in the network.
引用
收藏
页码:293 / 304
页数:12
相关论文
共 46 条
[41]   MECHANISMS UNDERLYING PATTERN GENERATION IN LOBSTER STOMATOGASTRIC GANGLION AS DETERMINED BY SELECTIVE INACTIVATION OF IDENTIFIED NEURONS .1. PYLORIC SYSTEM [J].
SELVERSTON, AI ;
MILLER, JP .
JOURNAL OF NEUROPHYSIOLOGY, 1980, 44 (06) :1102-1121
[42]   Phase-response curves and synchronized neural networks [J].
Smeal, Roy M. ;
Ermentrout, G. Bard ;
White, John A. .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2010, 365 (1551) :2407-2422
[43]   Modulation of stomatogastric rhythms [J].
Stein, Wolfgang .
JOURNAL OF COMPARATIVE PHYSIOLOGY A-NEUROETHOLOGY SENSORY NEURAL AND BEHAVIORAL PHYSIOLOGY, 2009, 195 (11) :989-1009
[44]   Red pigment concentrating hormone strongly enhances the strength of the feedback to the pyloric rhythm oscillator but has little effect on pyloric rhythm period [J].
Thirumalai, V ;
Prinz, AA ;
Johnson, CD ;
Marder, E .
JOURNAL OF NEUROPHYSIOLOGY, 2006, 95 (03) :1762-1770
[45]   A role for compromise: synaptic inhibition and electrical coupling interact to control phasing in the leech heartbeat CPG [J].
Weaver, Adam L. ;
Roffman, Rebecca C. ;
Norris, Brian J. ;
Calabrese, Ronald L. .
FRONTIERS IN BEHAVIORAL NEUROSCIENCE, 2010, 4
[46]   Relating network synaptic connectivity and network activity in the lobster (Panulirus interruptus) pyloric network [J].
Weaver, AL ;
Hooper, SL .
JOURNAL OF NEUROPHYSIOLOGY, 2003, 90 (04) :2378-2386