Associative-memory representations emerge as shared spatial patterns of theta activity spanning the primate temporal cortex.
Highly localized neuronal spikes in primate temporal cortex can encode associative memory; however, whether memory formation involves area-wide reorganization of ensemble activity, which often accompanies rhythmicity, or just local microcircuit-level plasticity, remains elusive. Using high-density electrocorticography, we capture local-field potentials spanning the monkey temporal lobes, and show that the visual pair-association (PA) memory is encoded in spatial patterns of theta activity in areas TE, 36, and, partially, in the parahippocampal cortex, but not in the entorhinal cortex. The theta patterns elicited by learned paired associates are distinct between pairs, but similar within pairs. This pattern similarity, emerging through novel PA learning, allows a machine-learning decoder trained on theta patterns elicited by a particular visual item to correctly predict the identity of those elicited by its paired associate. Our results suggest that the formation and sharing of widespread cortical theta patterns via learning-induced reorganization are involved in the mechanisms of associative memory representation.
Center for Transdisciplinary Research, Niigata University, Niigata-city, Niigata 951-8501, Japan.
Kiyoshi
K
Nakahara
Department of Bio-cybernetics, Faculty of Engineering, Niigata University, Niigata-city, Niigata 950-2181, Japan.
Ken
K
Adachi
Department of Physiology, Niigata University School of Medicine, Niigata-city, Niigata 951-8501, Japan.
Keisuke
K
Kawasaki
Department of Neurosurgery, NTT Medical Center Tokyo, Shinagawa-ku, Tokyo 141-8625, Japan.
Takeshi
T
Matsuo
Department of Electrical and Electronic Information Engineering, Toyohashi University of Technology, Toyohashi-city, Aichi 441-8580, Japan.
Hirohito
H
Sawahata
ATR Computational Neuroscience Laboratories, Keihanna Science City, Kyoto 619-0288, Japan.
Kei
K
Majima
Research Institute for Diseases of Old Age, Juntendo University School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan.
Masaki
M
Takeda
Lab of Neuronal Development, Graduate School of Medical and Dental Sciences, Niigata University, Niigata-city, Niigata 951-8501, Japan.
Sayaka
S
Sugiyama
Department of Bio-cybernetics, Faculty of Engineering, Niigata University, Niigata-city, Niigata 950-2181, Japan.
Ryota
R
Nakata
Department of Bio-cybernetics, Faculty of Engineering, Niigata University, Niigata-city, Niigata 950-2181, Japan.
Atsuhiko
A
Iijima
Center for Transdisciplinary Research, Niigata University, Niigata-city, Niigata 951-8501, Japan.
Hisashi
H
Tanigawa
Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, and Osaka University, Suita-city, Osaka 565-0871, Japan.
Takafumi
T
Suzuki
ATR Computational Neuroscience Laboratories, Keihanna Science City, Kyoto 619-0288, Japan.|Graduate School of Informatics, Kyoto University, Kyoto-city, Kyoto 606-8501, Japan.
Yukiyasu
http://orcid.org/0000-0002-9300-8268
Y
Kamitani
Center for Transdisciplinary Research, Niigata University, Niigata-city, Niigata 951-8501, Japan.|Department of Physiology, Niigata University School of Medicine, Niigata-city, Niigata 951-8501, Japan.
Isao
I
Hasegawa
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D000069280:Electrocorticography; D004566:Electrodes; D005260:Female; D008568:Memory / Q000502:physiology*; D011323:Primates; D013028:Space Perception / Q000502:physiology*; D013647:Task Performance and Analysis; D013702:Temporal Lobe / Q000502:physiology*; D013826:Theta Rhythm / Q000502:physiology*