Local-Distributed Integration by a Novel Neuron Ensures Rapid Initiation of Animal Locomotion

被引:9
作者
Mullins, Olivia J. [1 ,2 ]
Hackett, John T. [2 ,3 ]
Friesen, W. Otto [1 ,2 ]
机构
[1] Univ Virginia, Dept Biol, Charlottesville, VA 22904 USA
[2] Univ Virginia, Neurosci Grad Program, Charlottesville, VA 22904 USA
[3] Univ Virginia, Dept Mol Physiol & Biol Phys, Charlottesville, VA 22904 USA
基金
美国国家科学基金会;
关键词
LEECH SUBESOPHAGEAL GANGLION; CENTRAL PATTERN GENERATOR; CENTRAL-NERVOUS-SYSTEM; SWIMMING ACTIVITY; MEDICINAL LEECH; SPIKE INITIATION; ESCAPE BEHAVIOR; INTERSEGMENTAL COORDINATION; IMPULSE PROPAGATION; HIRUDO-MEDICINALIS;
D O I
10.1152/jn.00507.2010
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Mullins OJ, Hackett JT, Friesen WO. Local-distributed integration by a novel neuron ensures rapid initiation of animal locomotion. J Neurophysiol 105: 130-144, 2011. First published October 27, 2010; doi:10.1152/jn.00507.2010. Animals are adapted to respond quickly to threats in their environment. In many invertebrate and some vertebrate species, the evolutionary pressures have resulted in rapidly conducting giant axons, which allow short response times. Although neural circuits mediating escape behavior are identified in several species, little attention has been paid to this behavior in the medicinal leech, a model organism whose neuronal circuits are well known. We present data that suggest an alternative to giant axons for the rapid initiation of locomotion. A novel individual neuron, cell E21, appears to be one mediator of this short-latency action in the leech. In isolated nerve cord and semi-intact preparations, cell E21 excitation initiates and extends swimming and reduces the cycle period. The soma of this cell is located caudally, but its axon extends nearly the entire length of the nerve cord. We found that cell E21 fires impulses following local sensory inputs anywhere along the body and makes excitatory synapses onto the gating cells that drive swimming behavior. These distributed input-output sites minimize the distance information travels to initiate swimming behavior, thus minimizing the latency between sensory input and motor output. We propose that this single cell E21 functions to rapidly initiate or modulate locomotion through its distributed synaptic connections.
引用
收藏
页码:130 / 144
页数:15
相关论文
共 78 条
[41]   NEURONAL CONTROL OF SWIMMING IN MEDICINAL LEECH .1. DYNAMICS OF SWIMMING RHYTHM [J].
KRISTAN, WB ;
STENT, GS ;
ORT, CA .
JOURNAL OF COMPARATIVE PHYSIOLOGY, 1974, 94 (02) :97-119
[42]   COMMAND NEURON CONCEPT [J].
KUPFERMANN, I ;
WEISS, KR .
BEHAVIORAL AND BRAIN SCIENCES, 1978, 1 (01) :3-10
[43]   Bistable behavior originating in the axon of a crustacean motor neuron [J].
Le, T ;
Verley, DR ;
Goaillard, JM ;
Messinger, DI ;
Christie, AE ;
Birmingham, JT .
JOURNAL OF NEUROPHYSIOLOGY, 2006, 95 (03) :1356-1368
[44]   Phase relationships between segmentally organized oscillators in the leech heartbeat pattern generating network [J].
Masino, MA ;
Calabrese, RL .
JOURNAL OF NEUROPHYSIOLOGY, 2002, 87 (03) :1572-1585
[45]   Encoding of Oscillations by Axonal Bursts in Inferior Olive Neurons [J].
Mathy, Alexandre ;
Ho, Sara S. N. ;
Davie, Jenny T. ;
Duguid, Ian C. ;
Clark, Beverley A. ;
Haeusser, Michael .
NEURON, 2009, 62 (03) :388-399
[46]   ACTIVATION OF FICTIVE SWIMMING BY ELECTRICAL MICROSTIMULATION OF BRAIN-STEM LOCOMOTOR REGIONS IN AN INVITRO PREPARATION OF THE LAMPREY CENTRAL NERVOUS-SYSTEM [J].
MCCLELLAN, AD ;
GRILLNER, S .
BRAIN RESEARCH, 1984, 300 (02) :357-361
[47]  
MEYRAND P, 1992, J NEUROSCI, V12, P2803
[48]   PLASTICITY OF BEHAVIORAL-RESPONSE TO REPEATED INJECTION OF GLUTAMATE IN CUNEIFORM AREA OF RAT [J].
MITCHELL, IJ ;
REDGRAVE, P ;
DEAN, P .
BRAIN RESEARCH, 1988, 460 (02) :394-397
[49]   SITE-SPECIFIC POSTURAL AND LOCOMOTOR CHANGES EVOKED IN AWAKE, FREELY MOVING INTACT CATS BY STIMULATING THE BRAIN-STEM [J].
MORI, S ;
SAKAMOTO, T ;
OHTA, Y ;
TAKAKUSAKI, K ;
MATSUYAMA, K .
BRAIN RESEARCH, 1989, 505 (01) :66-74
[50]   COMPLEX MOTOR NEURON IN CRUSTACEA - 3 AXONAL SPIKE INITIATING ZONES IN 3 DIFFERENT GANGLIA [J].
MOULINS, M ;
VEDEL, JP ;
NAGY, F .
NEUROSCIENCE LETTERS, 1979, 13 (03) :231-236