RESEARCH NEUROSCIENCE sulcus (STS)and inferotemporal (T)corte A fast link between face perception and memory in the temporal pole hepooonaAel Sofia M.LandiPooja ViswanathanStephen Serene,Winrich A.Freiwald4 0 to faces th ere pers ded nonlinearly to stepwise imaging (fMRD).we localized areas TP cognizing someone we know requires Theories for the neural basis of person ree methods).We recorded responses from dating back to the id of t neu stores t出 men and how it link ne in the which spond t with a 205-im that in sider the case of r familiar)monkey faces (2 personally familiar ctivate the same person's me ry.We ory face cells in encoding facial info USA Th the eyes xtract facial identit tne s in th of n (F) uw.edu (S.ML) 9 D faces.(A)Schematic:Face per face M2 202: ethods)D right V. rs rostral to interaural lin 200ms ly.(D)Me us n als in spike (bottom).celresponds 30J20 1of5 NEUROSCIENCE A fast link between face perception and memory in the temporal pole Sofia M. Landi1,2*, Pooja Viswanathan1,3, Stephen Serene1 , Winrich A. Freiwald1,4* The question of how the brain recognizes the faces of familiar individuals has been important throughout the history of neuroscience. Cells linking visual processing to person memory have been proposed but not found. Here, we report the discovery of such cells through recordings from an area in the macaque temporal pole identified with functional magnetic resonance imaging. These cells responded to faces that were personally familiar. They responded nonlinearly to stepwise changes in face visibility and detail and holistically to face parts, reflecting key signatures of familiar face recognition. They discriminated between familiar identities, as fast as a general face identity area. The discovery of these cells establishes a new pathway for the fast recognition of familiar individuals. R ecognizing someone we know requires the combination of sensory perception and long-term memory. Where the brain stores these memories, and how it links sensory activity patterns to them, remains largely unknown. Consider the case of person recognition: The same person’s face can evoke vastly different retinal activity patterns, yet all activate the same person’s memory. We know how information from the eyes is transformed to extract facial identity across varying viewing conditions in the face-processing network (1), but not where and how this representation then activates person memory. Theories for the neural basis of person rec￾ognition have a long history in neuroscience dating back to the idea of the “grandmother neuron” in the 1960s, which would respond to any image of one’s grandmother and support the recollection of grandmother-related memories (2). A later theory posited a hybrid “face recog￾nition unit” (3), which would combine properties of sensory face cells in encoding facial information with properties of memory cells in storing infor￾mation from past personal encounters. Yet neither class of neuron has been found. Face cells and an entire network of face areas have been discovered in the superior temporal sulcus (STS) and inferotemporal (IT) cortex (1, 4, 5), and person memory cells have been discovered in the medial temporal lobe (6). How￾ever, in the temporal pole, only a few electro￾physiological recordings have been performed (7). With neuropsychological evidence pointing toward a role of this region in person recogni￾tion (8), and the recent discovery of a small subregion (temporal pole face area TP) selective for familiar faces (9), we decided to record from the temporal pole. Because face identity memo￾ries might be consolidated exactly where they are processed (10), we also recorded from the most identity-selective face area in the IT, the anterior￾medial face area (face area AM) (1,11) (Fig. 1A). Using whole-brain functional magnetic res￾onance imaging (fMRI), we localized areas TP and AM in the right hemispheres of two rhesus monkeys (Fig. 1, B and C, and fig. S1A; see methods). We recorded responses from all cells encountered. We assessed visual re￾sponsiveness, visual selectivity, and familiarity selectivity with a 205-image set that included human faces (30 personally familiar, 30 un￾familiar), monkey faces (12 personally familiar, RESEARCH Landi et al., Science 373, 581–585 (2021) 30 July 2021 1 of 5 1 Laboratory of Neural Systems, The Rockefeller University, New York, NY, USA. 2 Department of Physiology and Biophysics, University of Washington, Seattle, WA, USA. 3 The Nash Family Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, USA. 4 The Center for Brains, Minds & Machines, Cambridge, MA, USA. *Corresponding author. Email: slandi@uw.edu (S.M.L.); wfreiwald@rockefeller.edu (W.A.F.) Fig. 1. Cells in the temporal pole area TP respond to familiar faces. (A) Schematic: Face per￾ception systems are thought to feed into downstream face memory systems (3) in ways yet unknown. Candidate areas in the macaque brain are area AM and area TP. (B) Structural MRI (T1-weighted image) and functional overlay (faces > objects), color coded for negative common logarithm of p value (p < 0.001, uncorrected) showing electrodes targeting recording TP in monkeys M1 and M2 (see methods). D, dorsal; L, left; R, right; V, ventral. (C) Coronal (left), parasagittal (middle), and axial (right) slices showing TP in M1 and M2. Numbers indicate stereotaxic coordinates: millimeters rostral to interaural line, millimeters from midline to the right, and millimeters dorsal from inter￾aural line, respectively. (D) Mean peristimulus time histograms of two TP example cells (left M1, right M2) across the 205-stimuli set (FOF) in eight categories (top to bottom, far right) presented for 200 ms (bottom) with 500-ms interstimulus intervals in spikes per second (color scale bottom). Each cell responds significantly to a range of familiar monkey faces. Sparseness indexes (S) (see methods) are shown in the top right of each plot. A TP example cell (M2) C Perception Face processing TP AM sts amts 0 30 spikes/s 1 30 TP example cell (M1) 43 98 160 185 200 205 58 0 80 spikes/s 200 ms Stimulus on Personally familiar Unfamiliar ? B 2 10 R L D V M1 TP M2 TP Memory Face recognition units M1 M2 +26 +18 +3 +27 +18 +2 DStimulus index S=0.44 S=0.71 Downloaded from https://www.science.org at Southern Medical University on May 08, 2022