Anatomical Connections of the Functionally Defined "Face Patches" in the Macaque Monkey

Neuron

Volumn 90, Issue 6, 2016, Pages 1325-1342

  Grimaldi, Piercesare ^a,c   Saleem, Kadharbatcha S ^b   Tsao, Doris ^a  

^a California Institute of Technology   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CLAUSTRUM; CONTROLLED STUDY; FACIAL RECOGNITION; FEEDBACK SYSTEM; FEEDFORWARD SYSTEM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MACACA; MALE; MEDIAL TEMPORAL LOBE; NERVE CELL NETWORK; NEUROANATOMY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PULVINAR; REGULATORY MECHANISM; TEMPORAL LOBE; VISUAL STIMULATION; ANIMAL; BASAL GANGLION; FACE; MACACA FASCICULARIS; NEUROANATOMICAL TRACT TRACING; PHYSIOLOGY; RECOGNITION; RHESUS MONKEY; VISUAL CORTEX; VISUAL SYSTEM;

AMYGDALA; ANIMALS; BASAL GANGLIA; FACE; MACACA FASCICULARIS; MACACA MULATTA; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; PREFRONTAL CORTEX; PULVINAR; RECOGNITION (PSYCHOLOGY); VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84973931756     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.05.009     Document Type: Article

References (66)

1. Adolphs R. Conceptual challenges and directions for social neuroscience. Neuron 2010, 65:752-767.
2. Baldauf D., Desimone R. Neural mechanisms of object-based attention. Science 2014, 344:424-427.
3. Borra E., Ichinohe N., Sato T., Tanifuji M., Rockland K.S. Cortical connections to area TE in monkey: hybrid modular and distributed organization. Cereb. Cortex 2010, 20:257-270.
4. Cheng K., Saleem K.S., Tanaka K. Organization of corticostriatal and corticoamygdalar projections arising from the anterior inferotemporal area TE of the macaque monkey: a Phaseolus vulgaris leucoagglutinin study. J. Neurosci. 1997, 17:7902-7925.
5. Chung K., Deisseroth K. CLARITY for mapping the nervous system. Nat. Methods 2013, 10:508-513.
6. Cox D., Meyers E., Sinha P. Contextually evoked object-specific responses in human visual cortex. Science 2004, 304:115-117.
7. Distler C., Boussaoud D., Desimone R., Ungerleider L.G. Cortical connections of inferior temporal area TEO in macaque monkeys. J. Comp. Neurol. 1993, 334:125-150.
8. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1991, 1:1-47.
9. Freedman D.J., Riesenhuber M., Poggio T., Miller E.K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 2001, 291:312-316.
10. Freiwald W.A., Tsao D.Y. Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science 2010, 330:845-851.
11. Gross C.G. Visual Functions of Inferotemporal Cortex. Handbook of Sensory Physiology 1972, 451-458. Springer. R. Jung (Ed.).
12. Gross C.G., Rocha-Miranda C.E., Bender D.B. Visual properties of neurons in inferotemporal cortex of the Macaque. J. Neurophysiol. 1972, 35:96-111.
13. Hama H., Kurokawa H., Kawano H., Ando R., Shimogori T., Noda H., Fukami K., Sakaue-Sawano A., Miyawaki A. Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain. Nat. Neurosci. 2011, 14:1481-1488.
14. Hama H., Hioki H., Namiki K., Hoshida T., Kurokawa H., Ishidate F., Kaneko T., Akagi T., Saito T., Saido T., Miyawaki A. ScaleS: an optical clearing palette for biological imaging. Nat. Neurosci. 2015, 18:1518-1529.
15. Haxby J.V., Gobbini M.I., Furey M.L., Ishai A., Schouten J.L., Pietrini P. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 2001, 293:2425-2430.
16. Hung C.P., Kreiman G., Poggio T., DiCarlo J.J. Fast readout of object identity from macaque inferior temporal cortex. Science 2005, 310:863-866.
17. Ishai A., Schmidt C.F., Boesiger P. Face perception is mediated by a distributed cortical network. Brain Res. Bull. 2005, 67:87-93.
18. Issa E.B., DiCarlo J.J. Precedence of the eye region in neural processing of faces. J. Neurosci. 2012, 32:16666-16682.
19. Kanwisher N., Yovel G. The fusiform face area: a cortical region specialized for the perception of faces. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2006, 361:2109-2128.
20. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 1997, 17:4302-4311.
21. Kiani R., Esteky H., Mirpour K., Tanaka K. Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. J. Neurophysiol. 2007, 97:4296-4309.
22. Kornblith S., Cheng X., Ohayon S., Tsao D.Y. A network for scene processing in the macaque temporal lobe. Neuron 2013, 79:766-781.
23. Kravitz D.J., Saleem K.S., Baker C.I., Ungerleider L.G., Mishkin M. The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn. Sci. 2013, 17:26-49.
24. Ku S.P., Tolias A.S., Logothetis N.K., Goense J. fMRI of the face-processing network in the ventral temporal lobe of awake and anesthetized macaques. Neuron 2011, 70:352-362.
25. Lafer-Sousa R., Conway B.R. Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat. Neurosci. 2013, 16:1870-1878.
26. Lewis J.W., Van Essen D.C. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 2000, 428:112-137.
27. Markov N.T., Misery P., Falchier A., Lamy C., Vezoli J., Quilodran R., Gariel M.A., Giroud P., Ercsey-Ravasz M., Pilaz L.J., et al. Weight consistency specifies regularities of macaque cortical networks. Cereb. Cortex 2011, 21:1254-1272.
28. Markov N.T., Ercsey-Ravasz M.M., Ribeiro Gomes A.R., Lamy C., Magrou L., Vezoli J., Misery P., Falchier A., Quilodran R., Gariel M.A., et al. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex 2014, 24:17-36.
29. Maunsell J.H., van Essen D.C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J. Neurosci. 1983, 3:2563-2586.
30. McMahon D.B., Jones A.P., Bondar I.V., Leopold D.A. Face-selective neurons maintain consistent visual responses across months. Proc. Natl. Acad. Sci. USA 2014, 111:8251-8256.
31. Mishkin M. A memory system in the monkey. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1982, 298:83-95.
32. Moeller S., Freiwald W.A., Tsao D.Y. Patches with links: a unified system for processing faces in the macaque temporal lobe. Science 2008, 320:1355-1359.
33. Mosher C.P., Zimmerman P.E., Gothard K.M. Response characteristics of basolateral and centromedial neurons in the primate amygdala. J. Neurosci. 2010, 30:16197-16207.
34. Ohayon S., Tsao D.Y. MR-guided stereotactic navigation. J. Neurosci. Methods 2012, 204:389-397.
35. Ohayon S., Freiwald W.A., Tsao D.Y. What makes a cell face selective? The importance of contrast. Neuron 2012, 74:567-581.
36. Pinsk M.A., DeSimone K., Moore T., Gross C.G., Kastner S. Representations of faces and body parts in macaque temporal cortex: a functional MRI study. Proc. Natl. Acad. Sci. USA 2005, 102:6996-7001.
37. Pitcher D., Dilks D.D., Saxe R.R., Triantafyllou C., Kanwisher N. Differential selectivity for dynamic versus static information in face-selective cortical regions. Neuroimage 2011, 56:2356-2363.
38. Polosecki P., Moeller S., Schweers N., Romanski L.M., Tsao D.Y., Freiwald W.A. Faces in motion: selectivity of macaque and human face processing areas for dynamic stimuli. J. Neurosci. 2013, 33:11768-11773.
39. Popivanov I.D., Jastorff J., Vanduffel W., Vogels R. Stimulus representations in body-selective regions of the macaque cortex assessed with event-related fMRI. Neuroimage 2012, 63:723-741.
40. Quiroga R.Q., Reddy L., Kreiman G., Koch C., Fried I. Invariant visual representation by single neurons in the human brain. Nature 2005, 435:1102-1107.
41. Rajimehr R., Young J.C., Tootell R.B. An anterior temporal face patch in human cortex, predicted by macaque maps. Proc. Natl. Acad. Sci. USA 2009, 106:1995-2000.
42. Remedios R., Logothetis N.K., Kayser C. Unimodal responses prevail within the multisensory claustrum. J. Neurosci. 2010, 30:12902-12907.
43. Rockland K.S., Pandya D.N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 1979, 179:3-20.
44. Saleem K.S., Logothetis N.K. A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates 2012, Academic Press. Second edition.
45. Saleem K.S., Tanaka K. Divergent projections from the anterior inferotemporal area TE to the perirhinal and entorhinal cortices in the macaque monkey. J. Neurosci. 1996, 16:4757-4775.
46. Saleem K.S., Tanaka K., Rockland K.S. Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. Cereb. Cortex 1993, 3:454-464.
47. Saleem K.S., Suzuki W., Tanaka K., Hashikawa T. Connections between anterior inferotemporal cortex and superior temporal sulcus regions in the macaque monkey. J. Neurosci. 2000, 20:5083-5101.
48. Saleem K.S., Price J.L., Hashikawa T. Cytoarchitectonic and chemoarchitectonic subdivisions of the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 2007, 500:973-1006.
49. Saleem K.S., Kondo H., Price J.L. Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J. Comp. Neurol. 2008, 506:659-693.
50. Saleem K.S., Miller B., Price J.L. Subdivisions and connectional networks of the lateral prefrontal cortex in the macaque monkey. J. Comp. Neurol. 2014, 522:1641-1690.
51. Sato T., Uchida G., Tanifuji M. Cortical columnar organization is reconsidered in inferior temporal cortex. Cereb. Cortex 2009, 19:1870-1888.
52. Scalaidhe S.P., Wilson F.A., Goldman-Rakic P.S. Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. Cereb. Cortex 1999, 9:459-475.
53. Shipp S. The functional logic of cortico-pulvinar connections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:1605-1624.
54. Srihasam K., Mandeville J.B., Morocz I.A., Sullivan K.J., Livingstone M.S. Behavioral and anatomical consequences of early versus late symbol training in macaques. Neuron 2012, 73:608-619.
55. Suzuki W., Saleem K.S., Tanaka K. Divergent backward projections from the anterior part of the inferotemporal cortex (area TE) in the macaque. J. Comp. Neurol. 2000, 422:206-228.
56. Tanaka K. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 1996, 19:109-139.
57. Tsao D.Y., Freiwald W.A., Knutsen T.A., Mandeville J.B., Tootell R.B. Faces and objects in macaque cerebral cortex. Nat. Neurosci. 2003, 6:989-995.
58. Tsao D.Y., Freiwald W.A., Tootell R.B.H., Livingstone M.S. A cortical region consisting entirely of face-selective cells. Science 2006, 311:670-674.
59. Tsao D.Y., Moeller S., Freiwald W.A. Comparing face patch systems in macaques and humans. Proc. Natl. Acad. Sci. USA 2008, 105:19514-19519.
60. Tsao D.Y., Schweers N., Moeller S., Freiwald W.A. Patches of face-selective cortex in the macaque frontal lobe. Nat. Neurosci. 2008, 11:877-879.
61. Ungerleider L.G., Galkin T.W., Desimone R., Gattass R. Cortical connections of area V4 in the macaque. Cereb. Cortex 2008, 18:477-499.
62. Van Essen D.C. Surface-based approaches to spatial localization and registration in primate cerebral cortex. Neuroimage 2004, 23(Suppl 1):S97-S107.
63. Webster M.J., Ungerleider L.G., Bachevalier J. Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. J. Neurosci. 1991, 11:1095-1116.
64. Webster M.J., Bachevalier J., Ungerleider L.G. Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. J. Comp. Neurol. 1993, 335:73-91.
65. Webster M.J., Bachevalier J., Ungerleider L.G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb. Cortex 1994, 4:470-483.
66. Yang B., Treweek J.B., Kulkarni R.P., Deverman B.E., Chen C.K., Lubeck E., Shah S., Cai L., Gradinaru V. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 2014, 158:945-958.