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Central pattern generator-driven efference copy couples eye movements with forelimb locomotion in mice

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HAL Id: hal-02413495

https://hal.archives-ouvertes.fr/hal-02413495

Submitted on 16 Dec 2019

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Central pattern generator-driven efference copy couples eye movements with forelimb locomotion in mice

F França de Barros, C Taillebuis, M. Manuel, H. Bras, D Combes, François Lambert, M. Beraneck

To cite this version:

F França de Barros, C Taillebuis, M. Manuel, H. Bras, D Combes, et al.. Central pattern generator- driven efference copy couples eye movements with forelimb locomotion in mice. 2019 annual meeting Society for Neurosciences, Oct 2019, Chicago, United States. �hal-02413495�

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Find us at

Presentation 062.11 1-INCC UMR 8002, 2-SPPIN UMR 8003, CNRS, Paris, France; 3-INT UMR 7289, CNRS, Marseille, France;

4-INCIA UMR 5287, CNRS, Bordeaux, France; 5-Univ. de Paris, France; 6-Univ. Bordeaux, France

Central pattern generator-driven efference copy

couples eye movements with forelimb locomotion in mice

F. França de Barros

1,5

, C. Taillebuis

1,5,6

, M. Manuel

2,5

, H. Bras

3

, D. Combes

4,6

, F. M. Lambert

4,6

, M. Beraneck

1,5

Eye movements during treadmill locomotion in precollicular premammillary decerebrated

Acknowledgments

Work funded by the French entities: Agence Nationale de la Recherche (ANR) and the Centre National de la Recherche

Scientifique (CNRS).

We also thank Université de Paris and Bordeaux and the technical support provided by Patrice Jegouzo.

5 s 4 Hz

4Hz

5 s

-1.0 0.0 +1.0

Time(s)

-1.0 0.0 +1.0

Time(s) C8

Right

CN VI Left

CN VI

LeftC8 Right

C8

LeftL5 Right

L5

Right CN VI CN VILeft

Right C8 LeftC8

Right L5

n= 10 cycles

n= 10 cycles S1

Right

CN VI Left

CN VI

Right

C8 Left

C8

Right CN VI CN VILeft Right

C8 LeftC8 LeftL5

Sacral S1 stimulation - Lumbar CPG activation

1. The extra-ocular activity is coupled to fictive locomotion

Cervical C8 stimulation - Cervical CPG activation

Ex vivo recordings of the eye’s motor nuclei and locomo- tor CPGs in brainstem-spinal cord preparations of

neonatal mice

Ctrl Section 0

50 100

0.0 0.2 0.4 0.6 0.8

0.0 0.2 0.4 0.6 0.8 1.0

Ctrl Section

ns

5 s 5 s 5 s

r²=0.96

r²=0.99

S1

Control After full-cut midthoracic

S1 stim. S1 stim. C8 stim.

Right

CN VI Left

CN VI

LeftC8 C8

CN VILeft LeftC8 Right CN VI

LeftL2 LeftL2

Absolute Latency(ms)

CN VI vs C8

Ipsilateral Contralateral C8 Frequency(Hz)

CN VI Frequency(Hz)

Lumbar CPG activation Lumbar CPG activation Cervical CPG activation

2. Blocking the cervical locomotor network removes the spino-extraocular coupling

3. The cervical locomotor network is sufficient to produce the spino-extraocular coupling

Control 0 Ca2+ Washout

-In dark

- Head-fixed

-Motorized treadmill

1. Locomotion: treadmill induced a trot-like pattern.

0 2 4 6 8 10

0 2 4 6 8 10

Forepaw IF(Hz)

HindpawIF(Hz)

0 2 4 6 8 10

0 2 4 6 8 10

Forepaw IF(Hz)

HindpawIF(Hz)

R=0.4715 R=0.2333

R=0.7746 R=0.2620 R=-0.1494

180 0

2. Eyes: conjugated eye movements are correlated and in phase

0 2 4 6 8 10

0 2 4 6 8 10

Forepaw IF(Hz)

EyeHorizontalIF(Hz)

R= 0.4224

0 2 4 6 8 10

0 2 4 6 8 10

Forepaw IF(Hz)

EyeHorizontalIF(Hz)

0 2 4 6 8 10

0 2 4 6 8 10

Hind paw IF(Hz)

EyeHorizontalIF(Hz)

3. Coupling characteristics between limbs and eyes

0

0 2 4 6 180

0 2 4 6

Right eye IF(Hz)

LefteyeIF(Hz)

R=0.8871

3 2.25 1.5 0.75

180 0

Forepaw vs eye horizontal Right eye vs left eye

Forepaw vs hind paw

0

180

1s

Amplitude(°) Velocity(°/s)

Rational

Efference copies are neural replicas of motor outputs used to anticipate the sensory consequences of a self-generated motor action.

They are responsible for the coordination of motor beha- viors by generating intrinsic feed-forward signals that directly connect a local motor circuitry with another local circuitry involved in another motor behaviour.

An example of a predictive motor efference copy is the signal originating from the locomotor spinal CPG that is simultaneously responsible for tail ondulation as well as for driving eye movements during swimming in the Xenopus tadpole.

Study whether the CPG-driven predictive signal cou- pling eye movements to locomotion is preserved in mammals.

Credit: F.Lambert

1. Ex vivo: rhythmic coupled discharge was found between limb and abducens motor nerve activity during fictive

locomotion events elicited by both electrical and pharmacological stimulation.

2. In vivo: in absecbe of visual and vestibular inputs, conju- gated eye movements are coupled to locomotion were recorded, suggesting that the efference copy particpiates in gaze stabilization during viogorus locomotion.

3. Anatomy: rabies virus injection revealed ipsilateral monosynaptic ascending spinal connection from the cervi- cal with abducens motoneurons.

Conclusion Aim

Neuronal substrates of the spino-extraocular pathway

55h

infection Monosynaptic tracing Migration

7547 µm ±1798 Rabies virus in

lateral rectus muscle

nVI nVII g7

*

50 µm 50 µm

RVChAT Hoescht

RVChAT Hoescht

RVChAT

ChATRV Hoescht

cc

cc cc

50 µm 50 µm

C1-2

C3-4

C5-6

C7-8

C7-8

T1-2

nVII

0 5 10 15

0 10 20 30 40 50

Infected MNs

InfectedINs

LOCOMOTION

128 130 132 134 136 138 140 142 144 146 148 150 152 154 164156 158 160 162

Left

Forepaw Stance Swing

5sec

5deg Left eye

Hor pos

2deg 200ms Right eye

Hor pos

Left Right Treadmill ON

10cm/s

5deg

Injection of Rabies virus in the lateral rectus of adult mice:

1. Infected (RV+) motorneurons (ChAT labelling) in the abducens nucleus(nVI) ipsilateral to the injection.

2. RV+ interneurons are present all along the cervical (7547µm ± 1798).

3. On average, 1 infected MN in the nVI affects 6 INs in the cervical.

4. C7 shows an homogeneous bilateral infection; C2-C6 and C8 infected mostly ipsilaterally (68%).

C1 C2 C3 C4 C5 C6 C7 C8 0

2 4 6 8 10

InfectedINs Contralateral

Ipsilateral

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