1. LAMINAR DEVELOPMENT
How do V1 Ocular Dominance &Orientation maps develop?
Ocular dominance columns and orientation tuningare found before eye opening in the cat
How do cortical columns form?
Consistent tuning in vertical V1 penetrations beforeinterlaminar cortical connections have matured
HYPOTHESIS: The Cortical Subplate
Model of laminar development
Subplate develops maps that are
taught to LGN-to-layer 4 connections
Subplate input guides layer 2/3
clustering
Subplate input guides layers 4 and
2/3 connections
Grinvald (http://www. weizmann.ac.il/brain/images/cubes.html)
2. ADULT ORGANIZATION OF V1
Ocular Dominance Columns (ODCs)
Alternating stripes of cortex respond preferentially
to visual inputs of each eye
R/L in Figure
Orientation Columns
A smooth pattern of changing orientation
preference
Organized in a pinwheel like fashion
( in Figure)
Horizontal projections
connect areas of same
ocular dominance
Horizontal projections
connect areas of similar
orientation preference
3. LATERAL CONNECTIONS IN V1
Clusters of lateral projections are found in the
supragranular and infragranular layers
Bosking et al., 1997
Retina
Oriented
Learns geniculocortical map
Unoriented
On Center / Off surround
Learns corticogenicular map
Random retinal activity
drives network before eye
opening
Subplate
LGN
7. MODEL SUBPLATE MAP
Orientation Map Learned in Subplate
Left
Monocular Stripes
Afferents compete for
territory
Monocular Layers
Conserved # synapses
Eyes are uncorrelated
Subplate
LGN
Ocular Dominance Map Learned in Subplate
Retina
Right
Subplate map is taught to Layer 4
Patterned visual inputs drive segregation ofON and OFF subfields in Layer 4 neurons
At stimulus edges, ON and OFF thalamic cells arespatially out of phase and thus anti-correlated
Left Right
Retina
LGN
Subplate
Layer 4
8. MODEL LAYER 4 MAP
Oriented
Learned Layer 4 map
emulates LGN-Subplatemap
Subplate activity guides
development of LGN to
Layer 4 connections
ON and OFF layersbecome equally active
when eyes open
When eyes open,
random retinal activity
is replaced by patterned
visual inputs
9. MODEL LAYER 2/3 MAP
Subplate guides horizontal connections
Retina
LGN
Subplate
Left Right
Layer 2/3
Synapses with Subplate
in Layer 1
Clustered horizontal
connections
Layer 4 develops
connections to 2/3
Subplate activity
instructs developmentof Layer 2/3 connections
On Center / Off surround
Random retinal activity
drives network before
eye opening
Layer 4
10. MODEL LGN-TO-SUBPLATE MAP
Orientation Columns
Ocular Dominance Columns
Ocular Dominance Columns
develop in subplate with
help of conservation of LGN
synapses
[plot of ocularity index]
Oriented cells self organize
in subplate
[Length shows degree of
orientation tuning and angle
shows prefered orientation]
11. QUANTIFICATION OF SUBPLATE
TUNING
Matrices of Weights
Feedforward pattern of
connections from the LGN
Receptive fields initialized as
weight noise
Oriented profiles develop
Peak Orientation
Network is probed with
stimuli of different orientation
Peak orientation is plotted
Length shows orientation
index
Orientation Tuning Curves
Orientation tuning curves
calculated for each cell
Most fit gaussian profile withhalfwidths ~30˚ for tuned cells
0.79 1.00
0.54 0.48
12. LEARNED LGN-TO-4 MAP
Subplate Layer 4
Ocular Dominance Columns
Orientation Columns
Maps in the Subplate are taught to Layer 4
13. RECIPROCAL CONNECTIONS
BETWEEN LGN & SUBPLATE
Oriented corticofugal connections match
orientation of V1 cells
LGN to Subplate
Subplate to LGN
Orientation same as LGN to
Subplate connections
Patterns are transferred to
the later developing layer 6
to LGN connections
Raw connection patterns
Data from monocular OFF
simulation
Weights are clearly oriented
Murphy et al., (1999)
Model Results
AFFERENTS FROM ON LAYERS
AFFERENTS FROM OFF LAYERS
14. ON/OFF IN LAYER 4
ON and OFF segregation when eyes open
Spatially offset ON & OFF cells fire to same edge
Anti-correlation drives segregated receptive fields
Significant diversity exists in arrangement of ON
and OFF subfields in cortical receptive fields
15. MODEL SUBPLATE ABLATION
Ocular Dominance Columns fail to develop
Orientation Tuning fails to develop
Some cells have a significant
tuning index but inspection of
the curves show no tuning
(Ghosh & Shatz 1992)
(Kanold et al., 2001)
16. LAYER 2/3 CLUSTERED
HORIZONTAL CONNECTIONS
Subplate Guides Horizontal Clusters
Reciprocal connections between layer 2/3 cells
Cluster precision due to local isotropic filters
Size and spacing due to size of filters
Noisy filters would result in more realistic pattern
Model Results
17. LAYER 4-TO-2/3 CONNECTIONS
Subplate Provides Vertical Correlations
Focused connections contrast with 2/3 clusters
Learning gated by layer 2/3 activity
Connections develop without use of distance bias
Model Results
18. BDNF AND SUBPLATE ABLATION
Subplate ablation increases cortical BDNF
Increase or Decrease of BDNF blocks ODC
BDNF affects release of Glutamate and GABA
Model insights: Parameters Matter
Increasing excitation reduces the selectivity of
cells by enlarging their receptive fields
Increasing inhibition reduces activity and
results in noisier receptive fields
Equally changing both excitation and inhibition
causes a shift in balance
Increasing total input can reduce network
activity since DOGs suppress uniform inputs
(Ghosh & Shatz, 1994)
(Cabelli et al., 1995, 1997)
(Berardi & Maffei, 1999)
19 OTHER MODELS
Most models are single layered
Other developmental models have not
demonstrated how vertical columns arise
Clustering in Layer 2/3 rarely addressed
The coordinated development of layer 2/3 horizontal
connections with maps of orientation and ocular
dominance has not previously been modeled
The subplate goes unnoticed
Our model is the first to use the subplate to explain
cortical development
LAMINART Model (Grossberg and Williamson 2001)
Demonstrates how patterned vision can refine
horizontal connections in Layer 2/3
After development these circuits generate
properties of adult perceptual grouping
The present model is consistent with these results
20. CONCLUSIONS
Subplate enables development of Columns
Learns Orientation and Ocular Dominance Maps
Teaches OR and ODC to Layer 4
Instructs clustering of Layer 2/3 connections
Guides growth of interlaminer connections
Removal of Subplate eliminates map formation
Eye opening segregates ON & OFF inputs
The introduction of patterned vision provides a
spatial anticorrelation of ON and OFF cells
Future Directions
Allow subplate to die
Develop layer 2/3 maps
Incorporate more realistic inhibitory circuit and
develop inhibitory connections
Generalizes model to other cortical areas, such as
A1 and extrastriate areas
21. REFERENCES
Albus, K., & Wolf, W. (1984). J Physiol , 348, 153-185.
Allendoerfer , K. L., & Shatz , C. J. (1994). Annu Rev Neurosci , 17,
185-218.
Bosking , W. H., Zhang, Y., Schofield, B., & Fitzpatrick, D. (1997).
J Neurosci , 17(6), 2112-2127.
Cook, P. M., Prusky , G., & Ramoa , A. S. (1999). Vis Neurosci ,
16(3), 491-501.
Crair, M. C., Horton, J. C., Antonini , A., & Stryker, M. P. (2001). J
Comp Neurol , 430(2), 235-249.
Ghosh , A., & Shatz , C. J. (1992).. Science, 255(5050), 1441-1443.
Ghosh , A., & Shatz , C. J. (1994). J Neurosci , 14(6), 3862-3880
Grossberg, S., & Williamson, J. R. (2001). Cereb Cortex, 11(1),
37-58.
Kanold , P.O., Kara, P., Reid, R.C., Shatz , C.J. (2001). Soc.
Neurosci . Abstr ., P27.16.
Murphy P.C., Duckett S.G., Sillito A.M.(1999). Science, 286,
1152-1154.
Yoshioka, T., Blasdel , G. G., Levitt , J. B., & Lund, J. S. (1996).
Cereb Cortex, 6(2), 297-310.
S upported in part by AF OS R , DAR P A, NS F , and ONR .
Crair et al., 2001
4. VISUAL DEVELOPMENT TIMELINE
OFF field bias
Cortical cells respond to negative contrast stimuli
76% at P8
Contralateral Bias
At P8 contralateral eye dominates
Horizontal Connections
ODCs project more to areas of same dominance thanother dominance
Iso-oriented areas project primarily to areas of similarorientation
~20-30% of projections to different “modules”
VisualCortex
Lateral
GeniculateNucleus
E37 E44 E51 E58 E65/P0 P7 P14 P21 P28
LGN axons
in Subplate
LGN axons in
cortical plate
(layers 5 and 6) LGN axons
in Layer 4
Ocular
dominance
columns
emerge
Orientation
selective
neurons
detectedCritical period
for visual
deprivation
Retinal ganglion
cell afferents in
LGN Retinogeniculate
afferents
segregate
LGN
cytoarchitechtonic
lamina differentiate
Albus & Wolf 1984
Crair et al., 2001
Molecular gradients provide a crude map
Epherins, Netrins, Semaphorins, Slit, etc.
Activity refines existing maps
Activity provides correlations between related cells
Retina TectumNasal Temporal Anterior Posterior
A Nasal-Temporal
gradient of Eph receptors
in retinal ganglion cells
interact with anterior to
posterior gradients of
repellant epherin ligand
in the Tectum. The result
is a crude retinotopic
map.
Normal Development ‡
Binocular Deprivation ‡
Monocular Deprivation ‡
Cook et al., 1999
LGN
5. DEVELOPMENTAL MECHANISMS
TTX
6. CORTICAL SUBPLATE
Cortical subplate forms circuit with LGN
LGN afferents wait in subplate for weeks before they
synapse in cortical plate (Ghosh & Shatz 1994)
Ablation of subplate stops map formation
When subplate is ablated, ocular dominance
columns fail to form (Ghosh & Shatz 1992)
Orientation tuning and orientation maps do not
develop after subplate ablation (Kanold et al., 2001)
Subplate connects to Layer 4 (Ghosh 1995)
Connections exist from subplate to Layer 4 when
LGN afferents begin to grow into Layer 4
Subplate connects to Layer 2/3
Subplate connects to Layer 1 (Allendoerfer & Shatz 1994)
Layer 2/3 has dendritic arborizations in Layer 1
Migrating Neuron
How Do Laminar Circuits Develop? The Role of the Cortical Subplate in the Development
and Laminar Coordination of Orientation and Ocular Dominance Maps in V1Aaron Seitz and Stephen Grossberg
Department of Cognitive and Neural Systems, Boston University, Boston, MA
[email protected] [email protected] http://www.cns.bu.edu/~aseitz
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