Spatial structure of neuronal receptive field in awake monkey secondary visual cortex (V2)

Contributed by Mu-ming Poo, January 6, 2016 (sent for review October 12, 2015; reviewed by Judith Hirsch and Doris Y. Tsao)
February 2, 2016
113 (7) 1913-1918

Significance

Using a computational method to analyze neuronal responses evoked by natural scene stimuli, we performed a comprehensive identification of secondary visual cortex (V2) neuronal receptive fields (RFs) and found several novel spatial structures of RFs. This approach imposes no assumption about the selectivity of the neurons, thus allowing a more objective search of RFs. Furthermore, by combining single-unit recording with optical imaging of intrinsic signals, we examined the spatial distribution of V2 neurons exhibiting different RFs, with respect to the V2 stripes defined previously by cytochrome oxidase staining. The identified V2 RFs could be explained by convergence of V1 neurons with well-known primary visual cortex RFs. This study illustrates that computational approach is useful for comprehensive RF identification in higher visual cortices.

Abstract

Visual processing depends critically on the receptive field (RF) properties of visual neurons. However, comprehensive characterization of RFs beyond the primary visual cortex (V1) remains a challenge. Here we report fine RF structures in secondary visual cortex (V2) of awake macaque monkeys, identified through a projection pursuit regression analysis of neuronal responses to natural images. We found that V2 RFs could be broadly classified as V1-like (typical Gabor-shaped subunits), ultralong (subunits with high aspect ratios), or complex-shaped (subunits with multiple oriented components). Furthermore, single-unit recordings from functional domains identified by intrinsic optical imaging showed that neurons with ultralong RFs were primarily localized within pale stripes, whereas neurons with complex-shaped RFs were more concentrated in thin stripes. Thus, by combining single-unit recording with optical imaging and a computational approach, we identified RF subunits underlying spatial feature selectivity of V2 neurons and demonstrated the functional organization of these RF properties.

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Acknowledgments

We thank Dr. Yunqing Wen, Dr. Hou Xu, Dr. Xiaodong Chen, Junjie Cai, Dr. Shude Zhu, Dr. Peichao Li, and Dr. Yu-Xi Fu for technical support and Dr. Haishan Yao and Dr. Wei Wang for comments. This work was supported by grants from Ministry of Science and Technology (973 Program, 2011CBA00400) and Chinese Academy of Sciences (Strategic Priority Research Program, XDB02020001).

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References

1
DH Hubel, MS Livingstone, Segregation of form, color, and stereopsis in primate area 18. J Neurosci 7, 3378–3415 (1987).
2
JB Levitt, DC Kiper, JA Movshon, Receptive fields and functional architecture of macaque V2. J Neurophysiol 71, 2517–2542 (1994).
3
M Ito, H Komatsu, Representation of angles embedded within contour stimuli in area V2 of macaque monkeys. J Neurosci 24, 3313–3324 (2004).
4
A Anzai, X Peng, DC Van Essen, Neurons in monkey visual area V2 encode combinations of orientations. Nat Neurosci 10, 1313–1321 (2007).
5
X Tao, et al., Local sensitivity to stimulus orientation and spatial frequency within the receptive fields of neurons in visual area 2 of macaque monkeys. J Neurophysiol 107, 1094–1110 (2012).
6
R von der Heydt, E Peterhans, G Baumgartner, Illusory contours and cortical neuron responses. Science 224, 1260–1262 (1984).
7
J Hegdé, DC Van Essen, Selectivity for complex shapes in primate visual area V2. J Neurosci 20, RC61 (2000).
8
J Freeman, CM Ziemba, DJ Heeger, EP Simoncelli, JA Movshon, A functional and perceptual signature of the second visual area in primates. Nat Neurosci 16, 974–981 (2013).
9
H Zhou, HS Friedman, R von der Heydt, Coding of border ownership in monkey visual cortex. J Neurosci 20, 6594–6611 (2000).
10
DS Marcus, DC Van Essen, Scene segmentation and attention in primate cortical areas V1 and V2. J Neurophysiol 88, 2648–2658 (2002).
11
TO Sharpee, Computational identification of receptive fields. Annu Rev Neurosci 36, 103–120 (2013).
12
MC-K Wu, SV David, JL Gallant, Complete functional characterization of sensory neurons by system identification. Annu Rev Neurosci 29, 477–505 (2006).
13
G Felsen, J Touryan, F Han, Y Dan, Cortical sensitivity to visual features in natural scenes. PLoS Biol 3, e342 (2005).
14
R de Boer, P Kuyper, Triggered correlation. IEEE Trans Biomed Eng 15, 169–179 (1968).
15
M Carandini, et al., Do we know what the early visual system does? J Neurosci 25, 10577–10597 (2005).
16
JH Friedman, W Stuetzle, Projection pursuit regression. J Am Stat Assoc 76, 817–823 (1981).
17
J Rapela, G Felsen, J Touryan, JM Mendel, NM Grzywacz, ePPR: A new strategy for the characterization of sensory cells from input/output data. Network 21, 35–90 (2010).
18
J Rapela, JM Mendel, NM Grzywacz, Estimating nonlinear receptive fields from natural images. J Vis 6, 441–474 (2006).
19
JH van Hateren, A van der Schaaf, Independent component filters of natural images compared with simple cells in primary visual cortex. Proc Biol Sci 265, 359–366 (1998).
20
JP Jones, LA Palmer, An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. J Neurophysiol 58, 1233–1258 (1987).
21
J Touryan, G Felsen, Y Dan, Spatial structure of complex cell receptive fields measured with natural images. Neuron 45, 781–791 (2005).
22
X Chen, F Han, M-M Poo, Y Dan, Excitatory and suppressive receptive field subunits in awake monkey primary visual cortex (V1). Proc Natl Acad Sci USA 104, 19120–19125 (2007).
23
DH Hubel, MS Livingstone, Complex-unoriented cells in a subregion of primate area 18. Nature 315, 325–327 (1985).
24
JS Baizer, DL Robinson, BM Dow, Visual responses of area 18 neurons in awake, behaving monkey. J Neurophysiol 40, 1024–1037 (1977).
25
MS Livingstone, DH Hubel, Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc Natl Acad Sci USA 79, 6098–6101 (1982).
26
RB Tootell, MS Silverman, RL De Valois, GH Jacobs, Functional organization of the second cortical visual area in primates. Science 220, 737–739 (1983).
27
JC Horton, Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philos Trans R Soc Lond B Biol Sci 304, 199–253 (1984).
28
KR Gegenfurtner, DC Kiper, SB Fenstemaker, Processing of color, form, and motion in macaque area V2. Vis Neurosci 13, 161–172 (1996).
29
S Shipp, S Zeki, The functional organization of area V2, I: Specialization across stripes and layers. Vis Neurosci 19, 187–210 (2002).
30
HD Lu, AW Roe, Functional organization of color domains in V1 and V2 of macaque monkey revealed by optical imaging. Cereb Cortex 18, 516–533 (2008).
31
HD Lu, G Chen, H Tanigawa, AW Roe, A motion direction map in macaque V2. Neuron 68, 1002–1013 (2010).
32
U Polat, CW Tyler, What pattern the eye sees best. Vision Res 39, 887–895 (1999).
33
AJ Bell, TJ Sejnowski, The “independent components” of natural scenes are edge filters. Vision Res 37, 3327–3338 (1997).
34
A Hyvärinen, M Gutmann, PO Hoyer, Statistical model of natural stimuli predicts edge-like pooling of spatial frequency channels in V2. BMC Neurosci 6, 12 (2005).
35
N Rubin, The role of junctions in surface completion and contour matching. Perception 30, 339–366 (2001).
36
H Lee, C Ekanadham, AY Ng, Sparse deep belief net model for visual area V2, eds Platt JC, Koller D, Singer Y, Roweis ST, Advances in Neural Information Processing Systems (Curran Associates, Red Hook, NY), Vol 20, pp 873–880. (2008).
37
S Saremi, TJ Sejnowski, TO Sharpee, Double-gabor filters are independent components of small translation-invariant image patches. Neural Comput 25, 922–939 (2013).
38
RW Rodieck, Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res 5, 583–601 (1965).
39
LG Ungerleider, M Mishkin, Two cortical visual systems. Analysis of Visual Behavior, eds DJ Ingle, MA Goodale, RJW Mansfield (MIT Press, Cambridge, MA), pp. 549–586 (1982).
40
EA DeYoe, DJ Felleman, DC Van Essen, E McClendon, Multiple processing streams in occipitotemporal visual cortex. Nature 371, 151–154 (1994).
41
CE Connor, SL Brincat, A Pasupathy, Transformation of shape information in the ventral pathway. Curr Opin Neurobiol 17, 140–147 (2007).
42
NK Logothetis, DL Sheinberg, Visual object recognition. Annu Rev Neurosci 19, 577–621 (1996).
43
DY Tsao, MS Livingstone, Mechanisms of face perception. Annu Rev Neurosci 31, 411–437 (2008).
44
JJ DiCarlo, D Zoccolan, NC Rust, How does the brain solve visual object recognition? Neuron 73, 415–434 (2012).
45
EA DeYoe, DC Van Essen, Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317, 58–61 (1985).
46
SW Kuffler, Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16, 37–68 (1953).
47
DH Hubel, TN Wiesel, Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160, 106–154 (1962).
48
HGJM Kuypers, MK Szwarcbart, M Mishkin, HE Rosvold, Occipitotemporal corticocortical connections in the rhesus monkey. Exp Neurol 11, 245–262 (1965).
49
DC Van Essen, WT Newsome, JH Maunsell, JL Bixby, The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections. J Comp Neurol 244, 451–480 (1986).
50
PH Schiller, JG Malpeli, The effect of striate cortex cooling on area 18 cells in the monkey. Brain Res 126, 366–369 (1977).
51
P Girard, J Bullier, Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. J Neurophysiol 62, 1287–1302 (1989).
52
LM Chen, et al., A chamber and artificial dura method for long-term optical imaging in the monkey. J Neurosci Methods 113, 41–49 (2002).
53
A Arieli, A Grinvald, H Slovin, Dural substitute for long-term imaging of cortical activity in behaving monkeys and its clinical implications. J Neurosci Methods 114, 119–133 (2002).
54
VZ Marmarelis, Nonlinear Dynamic Modeling of Physiological Systems (John Wiley & Sons, Inc., Hoboken, NJ). (2004).
55
T Sharpee, NC Rust, W Bialek, Analyzing neural responses to natural signals: Maximally informative dimensions. Neural Comput 16, 223–250 (2004).
56
D Smyth, B Willmore, GE Baker, ID Thompson, DJ Tolhurst, The receptive-field organization of simple cells in primary visual cortex of ferrets under natural scene stimulation. J Neurosci 23, 4746–4759 (2003).
57
SMN Woolley, PR Gill, FE Theunissen, Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain. J Neurosci 26, 2499–2512 (2006).
58
TO Sharpee, KD Miller, MP Stryker, On the importance of static nonlinearity in estimating spatiotemporal neural filters with natural stimuli. J Neurophysiol 99, 2496–2509 (2008).
59
P Li, et al., A motion direction preference map in monkey V4. Neuron 78, 376–388 (2013).
60
Y Xiao, R Rao, G Cecchi, E Kaplan, Improved mapping of information distribution across the cortical surface with the support vector machine. Neural Netw 21, 341–348 (2008).

Information & Authors

Information

Published in

The cover image for PNAS Vol.113; No.7
Proceedings of the National Academy of Sciences
Vol. 113 | No. 7
February 16, 2016
PubMed: 26839410

Classifications

Submission history

Published online: February 2, 2016
Published in issue: February 16, 2016

Keywords

  1. receptive field
  2. V2
  3. natural images
  4. stripes

Acknowledgments

We thank Dr. Yunqing Wen, Dr. Hou Xu, Dr. Xiaodong Chen, Junjie Cai, Dr. Shude Zhu, Dr. Peichao Li, and Dr. Yu-Xi Fu for technical support and Dr. Haishan Yao and Dr. Wei Wang for comments. This work was supported by grants from Ministry of Science and Technology (973 Program, 2011CBA00400) and Chinese Academy of Sciences (Strategic Priority Research Program, XDB02020001).

Authors

Affiliations

Lu Liu1
Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
University of Chinese Academy of Sciences, Shanghai 200031, China;
Liang She1
Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
University of Chinese Academy of Sciences, Shanghai 200031, China;
Ming Chen
Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
University of Chinese Academy of Sciences, Shanghai 200031, China;
Tianyi Liu
Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
Haidong D. Lu
Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
Present address: State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Yang Dan
Division of Neurobiology, Department of Molecular and Cell Biology, Howard Hughes Medical Institute, Helen Wills Neuroscience Institute, University of California, Berkeley, CA 94720
Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;

Notes

3
To whom correspondence should be addressed. Email: [email protected].
Author contributions: L.L., L.S., H.D.L., Y.D., and M.-m.P. designed research; L.L., L.S., M.C., and T.L. performed research; L.L., L.S., and M.C. analyzed data; L.L., L.S., Y.D., and M.-m.P. wrote the paper; and T.L. trained the monkey.
Reviewers: J.H., University of Southern California; and D.Y.T., California Institute of Technology.
1
L.L. and L.S. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Spatial structure of neuronal receptive field in awake monkey secondary visual cortex (V2)
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 7
    • pp. 1673-E942

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