Tuned geometries of hippocampal representations meet the computational demands of social memory

被引:22
作者
Boyle, Lara M. [1 ]
Posani, Lorenzo [2 ,3 ]
Irfan, Sarah [4 ]
Siegelbaum, Steven A. [1 ,3 ,5 ]
Fusi, Stefano [1 ,2 ,3 ,6 ]
机构
[1] Columbia Univ, Vagelos Coll Phys & Surg, Dept Neurosci, Irving Med Ctr, New York, NY 10027 USA
[2] Columbia Univ, Ctr Theoret Neurosci, New York, NY 10027 USA
[3] Columbia Univ, Zuckerman Mind Brain Behav Inst, New York, NY 10027 USA
[4] Barnard Coll, New York, NY 10027 USA
[5] Columbia Univ, Vagelos Coll Phys & Surg, Irving Med Ctr, Dept Pharmacol, New York, NY 10032 USA
[6] Columbia Univ, Kavli Inst Brain Sci, New York, NY 10027 USA
关键词
INFORMATION-STORAGE; CA2; REGION; SYSTEMS; RECOLLECTION; RECOGNITION; RECALL; UNITS;
D O I
10.1016/j.neuron.2024.01.021
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Social memory consists of two processes: the detection of familiar compared with novel conspecifics and the detailed recollection of past social episodes. We investigated the neural bases for these processes using calcium imaging of dorsal CA2 hippocampal pyramidal neurons, known to be important for social memory, during social/spatial encounters with novel conspecifics and familiar littermates. Whereas novel individuals were represented in a low -dimensional geometry that allows for generalization of social identity across different spatial locations and of location across different identities, littermates were represented in a higher -dimensional geometry that supports high -capacity memory storage. Moreover, familiarity was represented in an abstract format, independent of individual identity. The degree to which familiarity increased the dimensionality of CA2 representations for individual mice predicted their performance in a social novelty recognition memory test. Thus, by tuning the geometry of structured neural activity, CA2 is able to meet the demands of distinct social memory processes.
引用
收藏
页码:1358 / 1371.e9
页数:24
相关论文
共 55 条
[1]   Social and novel contexts modify hippocampal CA2 representations of space [J].
Alexander, Georgia M. ;
Farris, Shannon ;
Pirone, Jason R. ;
Zheng, Chenguang ;
Colgin, Laura L. ;
Dudek, Serena M. .
NATURE COMMUNICATIONS, 2016, 7
[2]   Differential Relation between Neuronal and Behavioral Discrimination during Hippocampal Memory Encoding [J].
Allegra, Manuela ;
Posani, Lorenzo ;
Gomez-Ocadiz, Ruy ;
Schmidt-Hieber, Christoph .
NEURON, 2020, 108 (06) :1103-1112.e6
[3]  
AMIT DJ, 1989, MODELING BRAIN FUNCT
[4]   Place cells may simply be memory cells: Memory compression leads to spatial tuning and history dependence [J].
Benna, Marcus K. ;
Fusi, Stefano .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2021, 118 (51)
[5]   The Geometry of Abstraction in the Hippocampus and Prefrontal Cortex [J].
Bernardi, Silvia ;
Benna, Marcus K. ;
Rigotti, Mattia ;
Munuera, Jerome ;
Fusi, Stefano ;
Salzman, C. Daniel .
CELL, 2020, 183 (04) :954-+
[6]   The Code for Facial Identity in the Primate Brain [J].
Chang, Le ;
Tsao, Doris Y. .
CELL, 2017, 169 (06) :1013-+
[7]   A hypothalamic novelty signal modulates hippocampal memory [J].
Chen, Shuo ;
He, Linmeng ;
Huang, Arthur J. Y. ;
Boehringer, Roman ;
Robert, Vincent ;
Wintzer, Marie E. ;
Polygalov, Denis ;
Weitemier, Adam Z. ;
Tao, Yanqiu ;
Gu, Mingxiao ;
Middleton, Steven J. ;
Namiki, Kana ;
Hama, Hiroshi ;
Therreau, Ludivine ;
Chevaleyre, Vivien ;
Hioki, Hiroyuki ;
Miyawaki, Atsushi ;
Piskorowski, Rebecca A. ;
McHugh, Thomas J. .
NATURE, 2020, 586 (7828) :270-+
[8]   Ultrasensitive fluorescent proteins for imaging neuronal activity [J].
Chen, Tsai-Wen ;
Wardill, Trevor J. ;
Sun, Yi ;
Pulver, Stefan R. ;
Renninger, Sabine L. ;
Baohan, Amy ;
Schreiter, Eric R. ;
Kerr, Rex A. ;
Orger, Michael B. ;
Jayaraman, Vivek ;
Looger, Loren L. ;
Svoboda, Karel ;
Kim, Douglas S. .
NATURE, 2013, 499 (7458) :295-+
[9]  
Cymerblit-Sabba A., 2020, Recognition memory via repetition suppression in mouse hippocampal dorsal CA2 pyramidal neurons expressing the vasopressin 1b receptor, DOI [10.1101/2020.05.11.078915, DOI 10.1101/2020.05.11.078915]
[10]   Coding of social novelty in the hippocampal CA2 region and its disruption and rescue in a 22q11.2 microdeletion mouse model [J].
Donegan, Macayla L. ;
Stefanini, Fabio ;
Meira, Torcato ;
Gordon, Joshua A. ;
Fusi, Stefano ;
Siegelbaum, Steven A. .
NATURE NEUROSCIENCE, 2020, 23 (11) :1365-+