Larval zebrafish (Brachydanio rerio) are a popular model system because of their genetic attributes, transparency and relative simplicity. They have approximately 200 neurons that project from the brainstem into the spinal cord. Many of these neurons can be individually identified and laser-ablated in intact larvae. This should facilitate cellular-level characterization of the descending control of larval behavior patterns. Towards this end, we attempt to describe the range of locomotor behavior patterns exhibited by zebrafish larvae. Using high-speed digital imaging, a variety of swimming and turning behaviors were analyzed in 6- to 9-day-old larval fish. Swimming episodes appeared to fall into two categories, with the point of maximal bending of the larva's body occurring either near the mid-body (burst swims) or closer to the tail (slow swims). Burst swims also involved larger-amplitude bending, faster speeds and greater yaw than slow swims. Turning behaviors clearly fell into two distinct categories: fast, large-angle escape turns characteristic of escape responses, and much slower routine turns lacking the large counterbend that often accompanies escape turns. Prey-capture behaviors were also recorded. They were made up of simpler locomotor components that appeared to be similar to routine turns and slow swims. The different behaviors observed were analyzed with regard to possible underlying neural control systems. Our analysis suggests the existence of discrete sets of controlling neurons and helps to explain the need for the roughly 200 spinal-projecting nerve cells in the brainstem of the larval zebrafish.

Batty
R. S.
,
Blaxter
J. H. S.
 (
1992
).
The effect of temperature on the burst swimming performance of fish larvae
.
J. Exp. Biol
170
,
187
–.
Google Scholar
 
Bernhardt
R. R.
,
Chitnis
A. B.
,
Lindamer
L.
,
Kuwada
J. Y.
 (
1990
).
Identification of spinal neurons in the embryonic and larval zebrafish
.
J. Comp. Neurol
302
,
603
–.
Google Scholar
 
Bernstein
J. J.
,
Gelderd
J. B.
 (
1970
).
Regeneration of the long spinal tracts in the goldfish
.
Brain Res
20
,
33
–.
Google Scholar
 
Brockerhoff
S. E.
,
Hurley
J. B.
,
Janssen-Bienhold
U.
,
Neuhauss
S. C. F.
,
Driever
W.
,
Dowling
J. E.
 (
1995
).
A behavioral screen for isolating zebrafish mutants with visual system defects
.
Proc. Natl. Acad. Sci.USA
92
,
10545
–.
Google Scholar
 
Buchanan
J. T.
 (
1996
).
Lamprey spinal interneurons and their roles in swimming activity
.
Brain Behav. Evol
48
,
287
–.
Google Scholar
 
Coughlin
D. J.
 (
1994
).
Suction prey capture by clownfish larvae (Amphiprion perideraion)
.
Copeia
1
,
242
–.
Google Scholar
 
Coughlin
D. J.
,
Rome
L. C.
 (
1996
).
The roles of pink and red muscle in powering steady swimming in scup, Stenotomus chrysops
.
Am. Zool
36
,
666
–.
Google Scholar
 
Coughlin
D. J.
,
Strickler
J. R.
,
Sanderson
B.
 (
1992
).
Swimming and search behavior in clownfish, Amphiprion perideraion, larvae
.
Anim. Behav
44
,
427
–.
Google Scholar
 
De Graaf
F.
,
Van Raamsdonk
W.
,
Van Asselt
E.
,
Diegenbach
P. C.
 (
1990
).
Identification of motoneurons in the spinal cord of the zebrafish Brachydanio rerio with special reference to motoneurons that innervate intermediate muscle fibers
.
Anat. Embryol
182
,
93
–.
Google Scholar
 
Domenici
P.
,
Blake
R. W.
 (
1997
).
The kinematics and performance of fish fast-start swimming
.
J. Exp. Biol
200
,
1165
–.
Google Scholar
 
Eaton
R. C.
,
Bombardieri
R. A.
,
Meyer
D. L.
 (
1977
).
The Mauthner-initiated startle response in teleost fish
.
J. Exp. Biol
66
,
65
–.
Google Scholar
 
Eaton
R. C.
,
DiDomenico
R.
,
Nissanov
J.
 (
1991
).
Role of the Mauthner cell in sensorimotor integration by the brainstem escape network
.
Brain Behav. Evol
37
,
272
–.
Google Scholar
 
Eaton
R. C.
,
Emberley
D. S.
 (
1991
).
How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish
.
J. Exp. Biol
161
,
469
–.
Google Scholar
 
Eisen
J. S.
 (
1999
).
Patterning motoneurons in the vertebrate nervous system
.
Trends Neurosci
22
,
321
–.
Google Scholar
 
Faber
D. S.
,
Fetcho
J. R.
,
Korn
H.
 (
1989
).
Neuronal networks underlying the escape response in goldfish: general implications for motor control
.
Ann. N.Y. Acad. Sci
563
,
11
–.
Google Scholar
 
Fetcho
J. R.
 (
1987
).
A review of the organization and evolution of motoneurons innervating the axial musculature of vertebrates
.
Brain Res. Rev
12
,
243
–.
Google Scholar
 
Fetcho
J. R.
 (
1992
).
The spinal motor system in early vertebrates and some of its evolutionary changes
.
Brain Behav. Evol
40
,
82
–.
Google Scholar
 
Fetcho
J. R.
,
Cox
K.
,
O'Malley
D. M.
 (
1998
).
Monitoring activity in neuronal populations with single cell resolution in a behaving vertebrate
.
Histochem. J
30
,
153
–.
Google Scholar
 
Fetcho
J. R.
,
Faber
D. S.
 (
1988
).
Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish
.
J. Neurosci
8
,
4192
–.
Google Scholar
 
Fetcho
J. R.
,
Liu
K. S.
 (
1999
).
Zebrafish as a model system for studying neuronal circuits and behavior
.
Ann. N.Y. Acad.Sci
860
,
333
–.
Google Scholar
 
Fetcho
J. R.
,
O'Malley
D. M.
 (
1995
).
Visualization of active neural circuitry in the spinal cord of intact zebrafish
.
J. Neurophysiol
73
,
399
–.
Google Scholar
 
Fetcho
J. R.
,
O'Malley
D. M.
 (
1997
).
Imaging neuronal networks in behaving animals
.
Curr. Opin. Neurobiol
7
,
832
–.
Google Scholar
 
Fetcho
J. R.
,
Svoboda
K. R.
 (
1993
).
Fictive swimming elicited by electrical stimulation of the midbrain in goldfish
.
J. Neurophysiol
70
,
765
–.
Google Scholar
 
Foreman
M. B.
,
Eaton
R. C.
 (
1993
).
The direction change concept for reticulospinal control of goldfish escape
.
J. Neurosci
13
,
4101
–.
Google Scholar
 
Fraser
S.
,
Keynes
R.
,
Lumsden
A.
 (
1990
).
Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions
.
Nature
344
,
431
–.
Google Scholar
 
Fuiman
L. A.
,
Webb
P. W.
 (
1988
).
Ontogeny of routine swimming activity and performance in zebra danios (Teleostei: Cyprinidae)
.
Anim. Behav
36
,
250
–.
Google Scholar
 
Gillis
G. B.
 (
1998
).
Neuromuscular control of anguilliform locomotion: patterns of swimming in red and white muscle activity during swimming in the American eel Anguilla rostrata
.
J. Exp. Biol
201
,
3245
–.
Google Scholar
 
Grillner
S.
,
Wallen
P.
 (
1985
).
Central pattern generators forlocomotion, with special reference to vertebrates
.
Annu. Rev. Neurosci
8
,
233
–.
Google Scholar
 
Guthrie
S.
 (
1995
).
The status of the neural segment
.
Trends Neurosci
18
,
74
–.
Google Scholar
 
Hale
M. E.
 (
1996
).
The development of fast-start performance in fishes: Escape kinematics of the chinook salmon (Oncorhynchus tshawytscha)
.
Am. Zool
36
,
695
–.
Google Scholar
 
Harper
D. G.
,
Blake
R. W.
 (
1989
).
On the error involved in high-speed film when used to evaluate maximum accelerations of fish
.
Can. J. Zool
67
,
1929
–.
Google Scholar
 
Jayne
B. C.
,
Lauder
G. V.
 (
1996
).
New data on axial locomotion in fishes: how speed affects diversity of kinematics and motor patterns
.
Am. Zool
36
,
642
–.
Google Scholar
 
Kashin
S. M.
,
Feldman
A. G.
,
Orlovsky
G. N.
 (
1974
).
Locomotion of fish evoked by electrical stimulation of the brain
.
Brain Res
82
,
41
–.
Google Scholar
 
Kimmel
C. B.
,
Metcalfe
W. K.
,
Schabtach
E.
 (
1985
).
T-reticular interneurons: a class of serially repeating cells in the zebrafish hindbrain
.
J. Comp. Neurol
233
,
365
–.
Google Scholar
 
Lee
R. K. K.
,
Eaton
R. C.
 (
1991
).
Identifiable reticulospinal neurons of the adult zebrafish, Brachydanio rerio
.
J. Comp. Neurol
304
,
34
–.
Google Scholar
 
Lee
R. K. K.
,
Eaton
R. C.
,
Zottoli
S. J.
 (
1993
).
Segmental arrangement of reticulospinal neurons in the goldfish hindbrain
.
J. Comp. Neurol
329
,
539
–.
Google Scholar
 
Liu
K. S.
,
Fetcho
J. R.
 (
1999
).
Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish
.
Neuron
23
,
325
–.
Google Scholar
 
Livingston
C. A.
,
Leonard
R. B.
 (
1990
).
Locomotion evoked by stimulation of the brainstem in the Atlantic stingray, Dasyatis sabina
.
J. Neurosci
10
,
194
–.
Google Scholar
 
McClellan
A. D.
,
Grillner
S.
 (
1984
).
Activation of ‘fictive swimming’ by electrical microstimulation of the lamprey central nervous system
.
Brain Res
300
,
357
–.
Google Scholar
 
McClellan
A. D.
,
Hagevik
A.
 (
1997
).
Descending control of turning locomotor activity in larval lamprey: neurophysiology and computer modeling
.
J. Neurophysiol
78
,
214
–.
Google Scholar
 
Metcalfe
W. K.
,
Mendelson
B.
,
Kimmel
C. B.
 (
1986
).
Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva
.
J. Comp. Neurol
251
,
147
–.
Google Scholar
 
Morton
D. W.
,
Chiel
H. J.
 (
1994
).
Neural architectures for adaptive behavior
.
Trends Neurosci
17
,
413
–.
Google Scholar
 
Mos
W.
,
Roberts
B. L.
,
Williamson
R.
 (
1990
).
Activity patterns of motoneurons in the spinal dogfish in relation to changing fictive locomotion.
Phil. Trans. R. Soc. Lond. B
330
,
329
–
339.
Google Scholar
 
Müller
U. K.
,
Stamhuis
E. J.
,
Videler
J. J.
 (
2000
).
Hydrodynamics of unsteady fish swimming and the effects of body size: comparing the flow fields of fish larvae and adults
.
J. Exp. Biol
203
,
193
–.
Google Scholar
 
Nissanov
J.
,
Eaton
R. C.
 (
1989
).
Reticulospinal control ofrapid escape turning maneuvers in fishes
.
Am. Zool
29
,
103
–.
Google Scholar
 
Nissanov
J.
,
Eaton
R. C.
,
DiDomenico
R.
 (
1990
).
The motor output of the Mauthner cell, a reticulospinal command neuron
.
Brain Res
517
,
88
–.
Google Scholar
 
O'Malley
D. M.
,
Kao
Y.-H.
,
Fetcho
J. R.
 (
1996
).
Imaging the functional organization of zebrafish hindbrain segments
.
Neuron
17
,
1145
–.
Google Scholar
 
Nicolson
T.
,
Rusch
A.
,
Friedrich
R. W.
,
Granato
M.
,
Ruppersberg
J. P.
,
Nusslein-Volhard
C.
 (
1998
).
Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants
.
Neuron
20
,
271
–.
Google Scholar
 
Roberts
A.
,
Soffe
S. R.
,
Wolf
E. S.
,
Yoshida
M.
,
Zhao
F.-Y.
 (
1998
).
Central circuits controlling locomotion in young frog tadpoles
.
Ann. N.Y. Acad. Sci
860
,
19
–.
Google Scholar
 
Saint-Amant
L.
,
Drapeau
P.
 (
1998
).
Time course of the development of motor behaviors in the zebrafish embryo
.
J. Neurobiol
37
,
622
–.
Google Scholar
 
Siegel
J. M.
,
Tomaszewski
K. S.
 (
1983
).
Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye and other movements
.
J. Neurophysiol
50
,
696
–.
Google Scholar
 
Spierts
I. L. Y.
,
Van Leeuwen
J. L.
 (
1999
).
Kinematics and muscle dynamics of-and -starts of carp (Cyprinus carpio L.)
.
J. Exp. Biol
202
,
393
–.
Google Scholar
 
Svoboda
K. R.
,
Fetcho
J. R.
 (
1996
).
Interactions between the neural networks for escape and swimming in goldfish
.
J. Neurosci
16
,
843
–.
Google Scholar
 
Van Raamsdonk
W.
,
Bosch
T. J.
,
Smit-Onel
M. J.
,
Maslam
S.
 (
1996
).
Organization of the zebrafish spinal cord: distribution of motoneuron dendrites and 5-HT containing cells
.
Eur. J. Morph
34
,
65
–.
Google Scholar
 
Van Raamsdonk
W.
,
Maslam
S.
,
de Jong
D. H.
,
Smit-Onel
M. J.
,
Velzing
E.
 (
1998
).
Long term effects of spinal cord transection in zebrafish: swimming performances and metabolic properties of the neuromuscular system
.
Acta Histochem
100
,
117
–.
Google Scholar
 
Wardle
C. S.
,
Videler
J. J.
,
Altringham
J. D.
 (
1995
).
Tuning in to fish swimming waves: body form, swimming mode and muscle function
.
J. Exp. Biol
198
,
1629
–.
Google Scholar
 
Westerfield
M.
,
McMurray
J. V.
,
Eisen
J. S.
 (
1986
).
Identified motoneurons and their innervation of axial muscles in the zebrafish
.
J. Neurosci
6
,
2267
–.
Google Scholar
 
Zottoli
S. J.
 (
1977
).
Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish
.
J. Exp. Biol
66
,
243
–.
Google Scholar
 
This content is only available via PDF.
© 2000 by Company of Biologists
2000