Intro
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SC
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Architecture and models of the brain eye saccadic movement circuitry Benoˆıt Girard
[email protected] Institut des Syst` emes Intelligents et de Robotique (ISIR)
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Intro
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Plan 1
Introduction Eye Movements Saccades
2
Brainstem Saccade Generators Substrate Models
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Superior Colliculus Substrate Models
4
Basal Ganglia Substrate Models
5
Cortex Substrate Models
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Intro
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Plan 1
Introduction Eye Movements Saccades
2
Brainstem Saccade Generators Substrate Models
3
Superior Colliculus Substrate Models
4
Basal Ganglia Substrate Models
5
Cortex Substrate Models
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Intro
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Oculomotor Movements Numerous circuits, at all the levels of the CNS. Repertoire of movements / repertoire of (relatively) distinct systems : Stabilization : Vestibulo-ocular reflex (VOR), Opto-kinetic reflex/nystagmus (OKN).
Fovea-specific : Saccades, Smooth pursuit.
Vergence.
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Extra-ocular muscles organization
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Saccades
(Yarbus, 1967)
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Neural Substrate SEF LIP FEF
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BG SC Retinal Input Extraocular Muscles
Verm SBG
Intro
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Neural Substrate
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Intro
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Plan 1
Introduction Eye Movements Saccades
2
Brainstem Saccade Generators Substrate Models
3
Superior Colliculus Substrate Models
4
Basal Ganglia Substrate Models
5
Cortex Substrate Models
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Intro
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Neural Substrate MN :
oculomotor (III), trochlear (IV) and abducens (VI) nuclei
EBN , IBN : H : paramedian pontine reticular formation (PPRF), medular reticular formation (Med. RF) V : Rostral interstitial nucleus of medial longitudinal fasciculus (riMLF), nucleus of the posterior commissure (nPC)
TN : RIP
H : nucleus prepositus hypoglossi (NPH), medial vestibular nucleus (MVN), V : nucleus interstitial of Cajal (NIC)
OPN :
nucleus raphe interpositus (nRIP)
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Neural Substrate Left
Right
FX
FX
deep superior colliculus
deep superior colliculus
BN BUN
BN BUN
SC Burst Neurons (BN) SC Build−Up Neurons (BUN) SC Fixation Neurons (FX) cMRF
cMRF visuo−motor neurons
cMRF LLBN
dorsal Long−Lead Burst Neurons Neurons (LLBN) Omnipause Neurons (OPN) Long−Lead Burst Neurons (LLBN) Short Lead Excitatory Burst Neurons (EBN) Nucleus Prepositus Tonic Neurons (nph) Abducens Motor/Internuclear Neurons (MN) Inhibitory Burst Neurons (IBN)
OPN
LLBN
LLBN
EBN
R L
EBN
nph
nph
MN
MN
IBN
Eye Position
LLBN
IBN
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(Robinson, 1975) Feedback control of the saccade (as pertubed saccades have correct metrics).
Target Position
EBN TN
MN
Problems : Cranio-centric coordinates, Oblique saccades.
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(J¨ urgens et al., 1981) Retino-centric coordinates : resettable integrator RI
Desired Displacement
EBN TN
Trigger
OPN Bias
Where is the RI ?
IBN
MN
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(Scudder, 1988) IFN r
Bias Desired Displacement wrt the right
LLB r
EBNr Bias
TN r
MN r
Plant r
IBNr Bias weak indirect trigger
OPN
Changed order of operations (integration in LLB and substraction) RI changed in IFN Resumed saccades after OPN stimulation Straight oblique saccades Pb with staircase saccades
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(Scudder, 1988) IFN r
Bias Desired Displacement wrt the right
LLB r
EBNr Bias
TN r
MN r
Plant r
TN l
MN l
Plant
IBNr Bias weak indirect trigger
OPN
IBNl Bias Desired Displacement wrt the left
LLB l
EBNl Bias
IFN l
Antagonist control
l
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(Moschovakis, 1994) Bias Desired Displacement
LLB
EBN TN
RI
Bias OPN
Latch
Upward generator : RI ! Reset specified (OPN), Keeps Scudder’s model good properties.
MN
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What if the feedback was somwhere else ? Where are the RI ? Are there RI ? The SC could be part of the feedback mechanism (we’ll discuss that soon). The Cerebellum could play a role in the feedback control of saccades ! (Lef`evre et al., 1998)
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Intro
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Plan 1
Introduction Eye Movements Saccades
2
Brainstem Saccade Generators Substrate Models
3
Superior Colliculus Substrate Models
4
Basal Ganglia Substrate Models
5
Cortex Substrate Models
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Layers
SEF LIP FEF
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BG SC Retinal Input Extraocular Muscles
Verm SBG
Visual neurons (V), Quasi-visual neurons (QV) : memory, Visu-motor neurons (VMB/VMP) Motor neurons (M) Fixation neurons (FIX)
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Layers
SEF LIP FEF
= Quasi Visual (?)
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= Burst Neurons
BG SC Retinal Input Extraocular Muscles
Verm
= Build−Up Neurons
SBG
= Burst Neurons
Visual neurons (V), Quasi-visual neurons (QV) : memory, Visu-motor neurons (VMB/VMP) Motor neurons (M) Fixation neurons (FIX)
F : Arm Movement Neurons (Werner, 1993)
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Maps
SEF LIP FEF
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BG SC Retinal Input
Verm SBG
Extraocular Muscles
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Logarithmic maps Macaque (Robinson, 1972 ; Ottes et al., 1986) 3 90
2 45
Y(mm)
1
0
0
−1 2
−2
−45
5 10 20
−3
0
1
X Y z+A +i = ln( ), with z = ↵ + i BX BY A
2
X(mm)
80 −90
40 3
4
5
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Linear maps Mouse (Dr¨ager & Hubel, 1976), Rat (Simino↵ et al., 1966)
↵ = X /bX and
= Y /bY
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Spatio-temporal transformation : the problem Saccade encoded as : Superior Colliculus Motor Map (BN and BUN)
de plitu Am 10°
40°
20°
SC map : a (stereotyped) bump of activity on a given location,
90°
N3
45°
N1
0°
N2
−45°
−90°
a
a
EBN t
EBN t
TN
Upward Saccade Generator
TN
MN
Leftward Saccade Generator
MN
Extra−ocular muscles
Polar Angle
5° 2°
SG : two bursts of varying intensities. STT : How to transform one code into another ?
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SC
STT : weighted sum (van Opstal & van Gisbergen, 1987)
SC Map
Rate Code
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STT : weighted sum (van Opstal & van Gisbergen, 1987)
SC Map
SC Map
SC Map
SC Map SC Map SC Map SC Map
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Rate Code
Rate Code
Rate Code
Rate Code
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SC-in-the-loop
What if the SC was in the feedback loop ?
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(Droulez and Berthoz, 1991) Up
Up target 1
30°
30°
target 1 ard
0°
w e to cad sac get 1 tar
s
30° Down
“Moving Hills” hypothesis
30°
0° Right
30° Down
target 2
30°
Right
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(Waitzman et al., 1991) RI
190sp/s
2α TLLB TLLB TLLB TLLB TLLB
1/α
MLB NI
Collicular Map OPN
MN
Plant
Latch
100sp/s
“Stationary Decreasing Hill” Inspired by correlation results between BN burst decrease and eye trajectory, Very similar to a (J¨ urgens et al., 1981) model.
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SC-NOT-in-the-loop
Well, it’s probably not... (Kato, Grantyn, Dalezios, Moschovakis, THE LOCAL LOOP OF THE SACCADIC SYSTEM CLOSES DOWNSTREAM OF THE SUPERIOR COLLICULUS, Neuroscience, 143 (2006) 319 –337)
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STT : normalized weighted sum (Lee, Rohrer & Sparks, 1988)
SC Map
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Rate Code /
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Intro
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STT : normalized weighted sum (Lee, Rohrer & Sparks, 1988)
SC Map
SC Map
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Rate Code
Rate Code /
/ average
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SC Map SC Map SC Map SC Map
SC Map
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Rate Code
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/
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SC
STT : normalized weighted sum (Lee, Rohrer & Sparks, 1988)
SC Map
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Rate Code /
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SC Map
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Rate Code / decreased
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increased
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STT : summation & saturation (Groh, 2001 ; Goossens & van Opstal, 2006 ; Tabareau et al., 2007)
Summation
SC Map SC Map
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STT : summation & saturation (Groh, 2001 ; Goossens & van Opstal, 2006 ; Tabareau et al., 2007)
Summation SC Map SC Map SC Map
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STT : summation & saturation (Groh, 2001 ; Goossens & van Opstal, 2006 ; Tabareau et al., 2007)
Summation SC Map SC Map SC Map SC Map
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STT : summation & saturation (Groh, 2001 ; Goossens & van Opstal, 2006 ; Tabareau et al., 2007)
Summation
Summation
SC Map SC Map SC Map SC Map
SC Map SC Map SC Map SC Map
t
t
average
Summation SC Map SC Map SC Map SC Map
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decreased
increased
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STT : summation & saturation (Groh, 2001 ; Goossens & van Opstal, 2006 ; Tabareau et al., 2007)
Summation
SC Map SC Map
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Summation SC Map SC Map SC Map SC Map
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Intro
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Plan 1
Introduction Eye Movements Saccades
2
Brainstem Saccade Generators Substrate Models
3
Superior Colliculus Substrate Models
4
Basal Ganglia Substrate Models
5
Cortex Substrate Models
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Intro
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Basal Ganglia - Anatomy
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TH BG
Motor circuits
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Basal Ganglia - Anatomy
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D1
Str
D2
STN
BG GPi/SNr
Motor circuits
Motor circuits
subcortical interconnected nuclei, common to vertebrates, involved in cortico-basal loops, but also in subcortical ones (with SC, CBLM, etc.)
GPe
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Basal Ganglia - Anatomy Limbic
Associative Sensory
Motor
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TH ventral to dorsal striatum
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Motor circuits
subcortical interconnected nuclei, common to vertebrates, involved in cortico-basal loops, but also in subcortical ones (with SC, CBLM, etc.)
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BG
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Basal Ganglia - Anatomy Limbic
Associative Sensory
Motor
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TH BG ventral to dorsal striatum
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BG
BG
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SC
subcortical interconnected nuclei, common to vertebrates, involved in cortico-basal loops, but also in subcortical ones (with SC, CBLM, etc.)
BG
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BG
TH
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Basal Ganglia - Physiology
Adapted from (Chevalier & Deniau, 1990)
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TH BG
Motor circuits
Generic role of selection Selection by Disinhibition, Reinforcement Learning ) Cortico-striatal plasticity, controlled by dopamine
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Basal Ganglia - Physiology
Adapted from (Chevalier & Deniau, 1990)
Generic role of selection Selection by Disinhibition, Reinforcement Learning ) Cortico-striatal plasticity, controlled by dopamine
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Basal Ganglia - Physiology
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TH BG VTA SNc
Motor circuits
Generic role of selection Selection by Disinhibition, Reinforcement Learning ) Cortico-striatal plasticity, controlled by dopamine
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Direct / Indirect Pathways
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Cortex
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Direct
Indirect
Striatum
GPe
GPi/SNr
STN
Thalamus
(Albin et al. 1989) (Berns & Sejnowski, 1996) Same o↵-center on-surround mechanism in recent direct/hyperdirect models (Leblois et al., 2006)
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1
0
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1 0
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Direct / Indirect Pathways
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Cortex
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Direct Striatum
Indirect GPe w=1
GPi/SNr
STN
Thalamus
(Albin et al. 1989) (Berns & Sejnowski, 1996) Same o↵-center on-surround mechanism in recent direct/hyperdirect models (Leblois et al., 2006)
1
w=1/N 1
0
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1 0
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Direct / Indirect Pathways
1
Cortex
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Direct Striatum
Indirect GPe w=1
GPi/SNr
STN w=−1
Thalamus
(Albin et al. 1989) (Berns & Sejnowski, 1996) Same o↵-center on-surround mechanism in recent direct/hyperdirect models (Leblois et al., 2006)
1
w=1/N 1
0
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1 0
f(
) = f(
)=0
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GPR Model (Gurney et al., 2001)
Frontal Cortex
1
Cortex
0
Saliences Selection D1
Control STN
D2
w=1
GPi/SNr
GPe
1
w=1 1
0
0
w=−1 Thalamus
Control inhibition
Output
1 0
f(
) = f(
)=0
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GPR Limitations Channel 1
0.7
Channel 2
0.7
Channels 3−6
0.7
0.6
0.6
0.6
0.5
0.5
0.5
0.4
0.4
0.4
0.3
0.3
0.3
* 0.2
0.2
0.1
0.1
0.0
0.0
−0.1
0
1
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Time(s)
7
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−0.1 10 0
0.2 0.1
*
0.0 1
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Time(s)
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−0.1 10 0
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10
Time(s)
* : Instability. With uniformly drawn inputs : the ⌧ winning channel is more inhibited than the rest level in 30% of the cases.
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GPR Limitations Channel 1
0.7
Channel 2
0.7
Channels 3−6
0.7
0.6
0.6
0.6
0.5
0.5
0.5
0.4
0.4
0.4
0.3
0.3
0.3
* 0.2
0.2
0.1
0.1
0.0
0.0
−0.1
0
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Time(s)
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−0.1 10 0
0.2 0.1
*
0.0 1
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Time(s)
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−0.1 10 0
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Time(s)
* : Instability. With uniformly drawn inputs : the ⌧ winning channel is more inhibited than the rest level in 30% of the cases.
Intro
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Contracting Basal Ganglia (CBG) Model (Girard et al., 2008) Basal Ganglia Cortex
D2 Str
GPe S Thalamus
FS
FC
D1 Str
TRN STN
Includes previously ignored connexions. Amplificatory thalamo-cortical loop. Selective amplification in the frontal cortex, strict selection of the subcortical targets. Numerous internal loops : stability ?
GPi/SNr
Disinhibition of channel 2
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Intro
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Structure Basal Ganglia
Basal Ganglia Cortex
D2 Str
D2 Str
GPe
GPe
S Thalamus
S Thalamus
FS
FC
TH
D1 Str
TRN STN
GPi/SNr
Disinhibition of channel 2
TH
FS
FC
D1 Str
TRN STN
O↵-center on-surround circuits, Negative Feedback to amplify contrast, Contraction conditions analytically defined (BG and TC), Numerical checking of the contraction of the whole.
GPi/SNr
Disinhibition of channel 2
Cortex
Intro
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Structure Basal Ganglia Cortex
D2 Str
GPe S Thalamus
FS
FC
D1 Str
TRN STN
GPi/SNr
Disinhibition of channel 2
TH
O↵-center on-surround circuits, Negative Feedback to amplify contrast, Contraction conditions analytically defined (BG and TC), Numerical checking of the contraction of the whole.
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Intro
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Contraction
BG module : 2
Basal Ganglia Cortex
GPe D1 ((1 + )wD1 wGPe ) + ((1
D2 Str
2
GPe D2 )wD2 wGPe )
