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Holistic bursting cells store long-term memory in auditory cortex.

ABSTRACT: The sensory neocortex has been suggested to be a substrate for long-term memory storage, yet which exact single cells could be specific candidates underlying such long-term memory storage remained neither known nor visible for over a century. Here, using a combination of day-by-day two-photon Ca2+ imaging and targeted single-cell loose-patch recording in an auditory associative learning paradigm with composite sounds in male mice, we reveal sparsely distributed neurons in layer 2/3 of auditory cortex emerged step-wise from quiescence into bursting mode, which then invariably expressed holistic information of the learned composite sounds, referred to as holistic bursting (HB) cells. Notably, it was not shuffled populations but the same sparse HB cells that embodied the behavioral relevance of the learned composite sounds, pinpointing HB cells as physiologically-defined single-cell candidates of an engram underlying long-term memory storage in auditory cortex.

SUBMITTER: Li R

PROVIDER: S-EPMC10703882 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Holistic bursting cells store long-term memory in auditory cortex.

Li Ruijie R Huang Junjie J Li Longhui L Zhao Zhikai Z Liang Susu S Liang Shanshan S Wang Meng M Liao Xiang X Lyu Jing J Zhou Zhenqiao Z Wang Sibo S Jin Wenjun W Chen Haiyang H Holder Damaris D Liu Hongbang H Zhang Jianxiong J Li Min M Tang Yuguo Y Remy Stefan S Pakan Janelle M P JMP Chen Xiaowei X Jia Hongbo H

Nature communications 20231207 1

The sensory neocortex has been suggested to be a substrate for long-term memory storage, yet which exact single cells could be specific candidates underlying such long-term memory storage remained neither known nor visible for over a century. Here, using a combination of day-by-day two-photon Ca<sup>2+</sup> imaging and targeted single-cell loose-patch recording in an auditory associative learning paradigm with composite sounds in male mice, we reveal sparsely distributed neurons in layer 2/3 of ...[more]

PMID: 38062015

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Project description:Behaviorally-relevant sounds such as conspecific vocalizations are often available for only a brief amount of time; thus, goal-directed behavior frequently depends on auditory short-term memory (STM). Despite its ecological significance, the neural processes underlying auditory STM remain poorly understood. To investigate the role of the auditory cortex in STM, single- and multi-unit activity was recorded from the primary auditory cortex (A1) of two monkeys performing an auditory STM task using simple and complex sounds. Each trial consisted of a sample and test stimulus separated by a 5-s retention interval. A brief wait period followed the test stimulus, after which subjects pressed a button if the sounds were identical (match trials) or withheld button presses if they were different (non-match trials). A number of units exhibited significant changes in firing rate for portions of the retention interval, although these changes were rarely sustained. Instead, they were most frequently observed during the early and late portions of the retention interval, with inhibition being observed more frequently than excitation. At the population level, responses elicited on match trials were briefly suppressed early in the sound period relative to non-match trials. However, during the latter portion of the sound, firing rates increased significantly for match trials and remained elevated throughout the wait period. Related patterns of activity were observed in prior experiments from our lab in the dorsal temporal pole (dTP) and prefrontal cortex (PFC) of the same animals. The data suggest that early match suppression occurs in both A1 and the dTP, whereas later match enhancement occurs first in the PFC, followed by A1 and later in dTP. Because match enhancement occurs first in the PFC, we speculate that enhancement observed in A1 and dTP may reflect top-down feedback. Overall, our findings suggest that A1 forms part of the larger neural system recruited during auditory STM.

Dataset Information

Holistic bursting cells store long-term memory in auditory cortex.

Publications

Holistic bursting cells store long-term memory in auditory cortex.

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