S"muli
Challenges
Background
Methods Orientation Tuning
Conclusion
Form-cue invariant second-order contrast envelope responses in macaque V2 G. Li1, Z. Wang2, Z. Yao2, N. Yuan2, V. Talebi1, J. Tan2, Y. Wang2, Y. Zhou2, C.L. Baker1
1McGill Vision Research, Dept Ophthalmology, McGill University, Montreal, QC, Canada 2School of Life Sciences, University of Science and Technology of China, Hefei, China
Supported by CIHR-‐NSFC China-‐Canada Joint Health Ini9a9ve Collabora9on grant (CCI-‐92217; NSFC-‐30811120423) to CB and to YZ.
Introduction • Natural images frequently contain oriented
boundaries defined by differences of luminance (1st-‐order), or of contrast or texture (2nd-‐order).
• 1st-‐order s9muli are thought to be detected by neural mechanisms ac9ng like a conven9onal linear filter.
• Detec9on of 2nd-‐order s9muli could be explained by a ‘filter-‐rec9fy-‐filter’ cascade.
-‐1st-‐stage filters are tuned to the fine scale of the texture. -‐rec9fied outputs drive a 2nd-‐stage, coarser scale linear filter. • 2nd-‐order processing has been widely studied in
human psychophysics (Landy & Graham, 2004). • In primates the neural substrate s9ll remains unclear.
Spatial Frequency Tuning
Monkey vs. Cat
Neurons In One Penetration
Spatial Frequency Tuning Properties
Orientation Tuning Properties
Sinewave gra9ngs and contrast modula9on (CM) envelopes s9muli were presented on a gamma-‐corrected CRT monitor, placed at a 114 cm distance.
• anesthe9zed and paralyzed monkeys (Macaca mula(a) -‐ (N2O, Propofol, Sufentanil) + (Gallamine triethiodide, Tubocurarine chloride) • careful refrac9on and ar9ficial pupils. • extracellular recording:
-‐ glass-‐coated tungsten electrodes (FHC): V1 -‐> white maeer -‐> V2 -‐ Michigan Probes (NeuroNexus): near lunate sulcus.
• single-‐unit (SU): isolated using Plexon Offline Sorter, quan9fied as average firing rates. • mul9-‐unit ac9vity (MUA): defined as events that exceeded 3-‐σ of the filtered raw data
(300 – 5KHz), quan9fied as average firing rates. • experiment protocol:
-‐ luminance gra9ngs: spa9al frequency, orienta9on, RF-‐mapping -‐ envelope (CM) s9muli: carrier spa9al frequency, orienta9on envelope spa9al frequency, orienta9on
• 51 visually responsive neurons, 22 were 2nd-‐order responsive.
Reference: Mareschal I & Baker CL (1999), Visual Neuroscience 16:527-‐540. Tanaka H and Ohzawa I (2009), J Neurophysiol 101:1444-‐1462. Landy MS and Graham N (2004), The Visual Neuroscience, Chapter 73:1106-‐1118 Hallum LE, Movshon JA (2011), SfN Abstr 694.19/NN14
SU
MUA
Op9mal Spa9al Frequency Op9mal Orienta9on
1. Ensure that responses to 2nd-‐order s9muli are not due to inadvertent ac9va9on of linear/luminance mechanisms.
2. Use s9muli that provide the analy9cal power to analyze the tuning proper9es of both early and late stage filtering.
CM envelopes were generated by mul9plica9on of two gra9ng paeerns: a sta9onary high spa9al frequency (fCarrier) gra9ng as the ‘carrier’ and a driping low spa9al frequency (fEnvelope) gra9ng as the ‘envelope’. In Fourier frequency domain, such CM s9muli consist of components all close to the ‘carrier’ spa9al frequency, with no energy at the ‘envelope’ spa9al frequency.
A neuron that responds to an envelope s9mulus in which all Fourier components are clearly outside its gra9ng frequency-‐selec9ve range, must have been responding to the envelope of the s9mulus as a result of nonlinear processing. The nonlinearity might occur: (1) aper the 1-‐st stage filter (2nd-‐order processing, F-‐R-‐F model), or (2) because of an early nonlinearity (before filters, e.g. s9muli ar9fact). -‐ if so, the envelope response would not be selec9ve for the carrier spa9al frequency.
Criteria for a “2nd-‐order responsive” neuron:
ü responds to an envelope (CM) s"mulus (blue). ü all the Fourier components of s"mulus are
clearly outside its luminance frequency-‐selec"ve range (black).
ü tuned to carrier spa"al frequency (red).
Electrophysiology Recording:
Spa9al frequency tuning curves of three envelope responsive neurons for luminance s9muli and CM s9muli (upper row à SU, boeom row à MUA). Each plot shows luminance spa9al frequency (black), envelope spa9al frequency (blue) and carrier spa9al frequency (red). • Neurons are clearly tuned for luminance,
envelope and carrier spa9al frequency. • Different neurons exhibited different op9mal
spa9al frequencies for luminance , envelope and carrier.
• The op9mal carrier spa9al frequencies were clearly dis9nct from the luminance gra9ng response range. Simple luminance gra9ngs produced liele or no response at such high frequencies.
• Neurons exhibited similar, but slightly different spa9al frequency tuning curves for luminance and envelope.
• MUA exhibited similar tuning curves as SUs.
Orienta9on polar plots for the same three neurons (showed above). Orienta9on tuning curves for luminance (black), envelope (blue) and carrier (red) are shown in different columns. • Neurons are clearly tuned for luminance,
envelope and carrier orienta9ons. • Envelope response polar plots were
usually very similar to the corresponding luminance polar plots (form-‐cue invariance).
• Carrier orienta9on could be very narrowly tuned.
• No clear rela9onship between the carrier orienta9on tuning and the corresponding luminance tuning.
• MUA exhibited similar tuning curves as SUs.
A par9cularly good penetra9on with many envelope responsive neurons recorded by tungsten electrode. • V2 was iden9fied by gray maeer (V1)-‐white
maeer-‐gray maeer (V2) transi9on. Tuning proper9es changed significantly from V1 to V2.
• The recep9ve fields were at 6-‐12° eccentricity. • S9muli were confined to the neurons’ classical
recep9ve fields. There was no clear rela9onship between envelope responsivity and surround suppression.
• The op9mal value of carrier spa9al frequency and orienta9on varied with depth independently of luminance and envelope tuning.
Scaeerplot of op9mal carrier spa9al frequency against the op9mal luminance spa9al frequency.
• 2nd-‐order envelope responsive neurons (filled squares) had a carrier-‐luminance ra9o higher than 5:1. • Some neurons (opened triangles) responded to CM’s with a carrier-‐luminance ra9o around 2:1, probably due
to surround modula9on (Tanaka & Ohzawa, 2009; Hallum & Movshon, 2011). • Most envelope-‐responsive neurons had higher op9mal spa9al frequency for envelopes than luminance.
Scaeerplot of op9mal envelope spa9al frequency against op9mal luminance spa9al frequency.
Scaeerplot of op9mal carrier spa9al frequency against op9mal envelope spa9al frequency.
MUA MUA MUA
Scaeerplot of op9mal envelope orienta9on against op9mal luminance orienta9on.
Scaeerplot of op9mal carrier orienta9on against op9mal luminance orienta9on.
• Envelope responsive neurons with high carrier-‐luminance ra9o (> 5:1, filled squares) cluster around the equality line (form-‐cue invariance); low ra9o neurons (opened triangles) are randomly distributed.
• There is no fixed rela9onship between the op9mal carrier and luminance (envelope) orienta9ons.
The op9mal carrier spa9al frequencies of monkey V2 are significantly higher than those for cat area 18 (p < 0.001, Mann-‐Whitney U test).
The carrier orienta9on tuning bandwidth of monkey V2 neurons is significantly narrower than in cat area 18 (p < 0.001, Mann-‐Whitney U test).
In monkey V2 neurons, the op9mal spa9al frequency is usually higher for envelopes than for luminance, but in cat area 18 it is usually lower.
l These results show that many macaque V2 neurons are selec9vely responsive to 2nd-‐order s9muli in a manner that cannot be explained by quasi-‐linear recep9ve fields, but which implies a specialized nonlinear mechanism.
l Unlike responses shaped by surround modula9on, these neurons exhibit form-‐cue invariant orienta9on selec9vity and also exhibit a high carrier-‐luminance ra9o (> 5:1).
l Form-‐cue invariant 2nd-‐order contrast envelope responsive neurons could provide a func9onally useful, explicit representa9on of segmenta9on boundaries.
SU
MUA
Cell 1 Cell 2 Cell 3 A
B
C
D
E
F
MUA Carrier Orienta9on Envelope Orienta9on Luminance Orienta9on
Cell 1
Cell 2
Cell 3
0.0
0.5
1.0
1.5
2.0
2.5
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Car
rier O
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atio
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(spi
kes/
sec)
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6
8
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Z0514
Lum
inan
ce M
odul
ated
Res
pons
e (s
pike
s/se
c)
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1
2
3
4
0
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6090
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0
1
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Z0514
Env
elop
e O
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(spi
kes/
sec)
0.0
0.5
1.0
1.5
0
30
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0.0
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1.0
1.5Z0504
Env
elop
e O
rient
atio
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nse
(spi
kes/
sec)
0.0
2.5
5.0
7.5
10.0
0
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2.5
5.0
7.5
10.0
Z0504
Lum
inan
ce M
odul
ated
Res
pons
e (s
pike
s/se
c)
0
1
2
3
0
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6090
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330
0
1
2
3
Z0504
Car
rier O
rient
atio
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nse
(spi
kes/
sec)
0
3
6
9
12
15
0
30
6090
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330
0
3
6
9
12
15
Z0517
Car
rier O
rient
atio
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espo
nse
(spi
kes/
sec)
0
3
6
9
12
15
0
30
6090
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0
3
6
9
12
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Z0517
Env
elop
e O
rient
atio
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espo
nse
(spi
kes/
sec)
0
5
10
15
20
0
30
6090
120
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240270
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0
5
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20
Z0517
Lum
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ce M
odul
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Res
pons
e (s
pike
s/se
c)
0
20
40
60
0
30
60
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330
0
20
40
60
Mul
tiUni
t Res
pons
e (s
pike
s/se
c)C
ontra
st M
odul
ated
0
60
120
180
180
120
60
Z0517
Lum. Carr. Env.
Mul
tiUni
t Res
pons
e (s
pike
s/se
c)Lu
min
ance
Mod
ulat
ed
0
100
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300
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100
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300
Mul
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t Res
pons
e (s
pike
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c)C
ontra
st M
odul
ated
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50
100
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100
50
Z0504
Lum. Carr. Env.
Mul
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pons
e (s
pike
s/se
c)Lu
min
ance
Mod
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100
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Mul
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pons
e (s
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c)C
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st M
odul
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25
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75
50
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Z0514
Z0514
Lum. Carr. Env. Illu. Con.
Mul
tiUni
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pons
e (s
pike
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c)Lu
min
ance
Mod
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MUA MUA
1st-‐order 2nd-‐order
narrow broad
cat data: Mareschal & Baker (1999)
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