RESEARCH I REPORT (face detection),human versus monkey faces inone small region of the temporal pole,other 34 y37657-676 26. 27.T.Mer C.R.Olson. faces(p.05,permutation tests;Fig .4D r in TP in TP an AM and the qualitative difre 0 le.B.Miner.Neurol.N fers (p> .1,pe hat 209 faces in TP and AM (Fig E and F).Onset ggio Castelo.M.I.Gobbini,PLOS ONE 10. ecific subset of short-latency AM cells 33. dpeak times 34 the lac 20 mutation tests:F ions 8.220-0 AM ape and ent eA rski's"gnostic unit"(),and Bruce an ould facilitat the fo (202) oung's fac 3537)a 381.Th s not allow for direct access without the need t KNOWLEDGMENTS y o Gros temporal pole of the face stem in a AM new cells are not fo REF 30.845-85 s both and on Thev shp (to P. emporal perso con cept cells (6)by a the t.M.从Cnun euroscl.17 ntties not by s (2) to WA 113017刀8-17 9 andi W.A freiwald Science 357.591-595 biec tand face recogniti ns and hav Barry.E. .5d.2.635-63 ion lictive norma ion.or sparsi n(9,25-29 effects resul f① are r n.Proc.Nat ent nu ally region()outside .A W.Your core object and fac J.W.Sh EMENTARY MATERIALS Ce/@ /6554/581//DC memory mecha Memory cons 25.S1o tl Acad Sol USA.112 te0,30.He that 20. .Cagno132262-268 amiliar conspeci andi et al Science 373,558(201) 30Juy202 (face detection), human versus monkey faces (species identification), and familiar versus unfamiliar monkey faces, human faces, and objects (semantic classification). Peak deco￾ding accuracy for face detection and species identification was higher for AM than TP (p < 0.05, permutation tests). The reverse was the case for semantic classification of monkey faces (p < 0.05, permutation tests; Fig. 4D), which seems to emerge faster in TP. How￾ever, we could not detect any significant latency differences between AM and TP for any of the binary classifiers (p > 0.1, permutation tests; Fig. 4D). Third, we analyzed the time courses of identity decoding between familiar monkey faces in TP and AM (Fig. 4, E and F). Onset and peak times for decoding familiar monkey identities were similar in both areas (p > 0.1, permutation tests; Fig. 4F). We report here the discovery of a new class of face memory cells. They share the conjunc￾tion of facial shape and familiarity selectivity with Lettvin’s grandmother cell hypothesis (2), Konorski’s “gnostic unit” (24), and Bruce and Young’s face recognition unit (3). TP differs, however, from the grandmother cell hypothe￾sis in that the identity of a familiar face is not represented by a single neuron but rather by a distributed population response. Although highly face selective, TP cells are qualitatively different from inferotemporal face cells, even those at the apex of the face-processing system in area AM (1, 11): The new cells are selective not for faces in general but for personally familiar ones, encode personally familiar faces both categorically and individually, and exhibit key functional character￾istics of face recognition. They also differ from mediotemporal person concept cells (6) by a much shorter response latency and selectivity toward the inner face. TP cells encode familiar face identities not by single cells—as the grand￾mother neuron concept (2) suggested—but as populations (24). Past studies have found that visual familiar￾ity with a stimulus reduces activity throughout object and face recognition systems and have described this reduction as repetition suppres￾sion, predictive normalization, or sparsifica￾tion (9, 25–29). These effects result primarily from repeated stimulus exposure. Our finding of (i) selective and specific response enhance￾ment (ii) that is robust across multiple trans￾formations (iii) in a spatially localized brain region (iv) outside of core object and face processing systems (v) as a result of personal real-life experience is a fundamentally different memory mechanism. Memory consolidation theories agree that long-term memories are stored in the cortex (10, 30). Here, we show that personal real-life experience has the astonishing capacity to carve out a small piece of cortex and consolidate very specific memories there. If familiar conspecific face memories are stored in one small region of the temporal pole, other modules with similar specificity probably exist nearby. More complex knowledge systems, for example, about individuals and their social relationships (31), may be built upon these foundations. This would explain person-related agnosia after damage to the temporal pole (8). TP signals face information surprisingly fast, which might explain the astonishing speed of familiar face recognition (32, 33). The simultaneity of familiar face processing in TP and AM and the qualitative differences in their selectivity—TP functionally mimics face recognition, whereas AM does not—suggest that AM and TP may operate functionally and possibly structurally in parallel. For example, a specific subset of short-latency AM cells may provide face-identity information to TP. Alter￾natively, in agreement with the lack of docu￾mented direct connections between AM and TP (34), there may be two pathways of face and person memory: one pathway from AM to a perirhinal face area (9), entorhinal cortex, and the hippocampus and a second pathway to TP. The first pathway would facilitate the formation of new associations (35–37) and the feeling of familiarity (38). The second pathway would allow for direct access—without the need to recapitulate all stages of the first pathway—to long-term semantic face information in the temporal pole. REFERENCES AND NOTES 1. W. A. Freiwald, D. Y. Tsao, Science 330, 845–851 (2010). 2. C. G. Gross, Neuroscientist 8, 512–518 (2002). 3. V. Bruce, A. Young, Br. J. Psychol. 77, 305–327 (1986). 4. D. I. Perrett, J. K. Hietanen, M. W. Oram, P. J. Benson, Philos. Trans. R. Soc. London Ser. B 335, 23–30 (1992). 5. N. Kanwisher, J. McDermott, M. M. Chun, J. Neurosci. 17, 4302–4311 (1997). 6. R. Q. Quiroga, L. Reddy, G. Kreiman, C. Koch, I. 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Unfamiliar face stimuli were obtained from the PrimFace database (https://visiome.neuroinf.jp/primface), which is funded by Grant-in-Aid for Scientific Research on Innovative Areas, “Face Perception and Recognition,” from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan. Funding: This work was supported by the Howard Hughes Medical Institute International Student Research Fellowship (to S.M.L.); the German Primate Centre Scholarship (to P.V.); the Simons Foundation Junior Fellowship (to P.V.); the Center for Brains, Minds & Machines funded by National Science Foundation STC award CCF-1231216; the National Eye Institute of the National Institutes of Health (R01 EY021594 to W.A.F.); the National Institute of Mental Health of the National Institutes of Health (R01 MH105397 to W.A.F.); the National Institute of Neurological Disorders and Stroke of the National Institutes of Health (R01NS110901 to W.A.F.); the Department of the Navy, Office of Naval Research under ONR award number N00014-20-1-2292; and The New York Stem Cell Foundation (to W.A.F.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Author contributions: Conceptualization: S.M.L., W.A.F. Data curation: S.M.L., S.S. Formal analysis: S.M.L. Investigation: S.M.L., P.V. Visualization: S.M.L., S.S. Funding acquisition: W.A.F. Writing – original draft: S.M.L., P.V., W.A.F. Writing – review and editing: S.M.L., P.V., S.S., W.A.F. Competing interests: The authors declare that they have no competing interests. Data and materials availability: There are no restrictions on data availability, and data are deposited on the FigShare repository (39). SUPPLEMENTARY MATERIALS science.sciencemag.org/content/373/6554/581/suppl/DC1 Materials and Methods Figs. S1 to S6 References (40–47) MDAR Reproducibility Checklist View/request a protocol for this paper from Bio-protocol. 24 March 2021; accepted 22 June 2021 Published online 1 July 2021 10.1126/science.abi6671 Landi et al., Science 373, 581–585 (2021) 30 July 2021 5 of 5 RESEARCH | REPORT Downloaded from https://www.science.org at Southern Medical University on May 08, 2022