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1.621000 四川 绵阳,四川中医药高等专科学校临床医学院诊断学教研室
2.621000 四川 绵阳,四川中医药高等专科学校医学基础部生理学教研室
[张维维,E-mail:weky_1981@163.comZHANG Weiwei, E-mail: weky_1981@163.com
收稿:2023-12-07,
修回:2024-02-26,
纸质出版:2024-08-30
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杨丹阳, 张维维. 痕迹性眨眼条件反射习得和巩固阶段海马中间神经元的放电活动变化[J]. 陆军军医大学学报, 2024,46(16):1874-1881.
Danyang YANG, Weiwei ZHANG. Changes in hippocampal interneuronal activity during acquisition and consolidation of trace eyeblink conditioning in mice[J]. Journal of Army Medical University, 2024, 46(16): 1874-1881.
杨丹阳, 张维维. 痕迹性眨眼条件反射习得和巩固阶段海马中间神经元的放电活动变化[J]. 陆军军医大学学报, 2024,46(16):1874-1881. DOI: 10.16016/j.2097-0927.202312040.
Danyang YANG, Weiwei ZHANG. Changes in hippocampal interneuronal activity during acquisition and consolidation of trace eyeblink conditioning in mice[J]. Journal of Army Medical University, 2024, 46(16): 1874-1881. DOI: 10.16016/j.2097-0927.202312040.
目的
2
研究小鼠背侧海马中间神经元在联合型记忆习得和巩固2个阶段的放电活动变化及其特征。
方法
2
以痕迹性眨眼条件反射(trace eyeblink conditioning
tEBC)作为联合型记忆行为模型
将18只野生型C57BL/6小鼠(雄性
10~12周龄
体质量22~25 g)通过简单随机抽样分为配对组(
n
=9)和假配对组(
n
=9)。配对组每天接受配对给予的条件刺激(conditioned stimulus
CS)和非条件刺激(unconditioned stimulus
US)
二者的配对关系为CS结束后250 ms给予US。假配对组每天接受同样数量的CS和US
但二者不存在时间上的配对关系。连续训练4 d
配对组小鼠建立tEBC
表现出条件眨眼反应(conditioned eyeblink response
CR)。在每天的训练过程中和训练后1.5 h
利用微电极阵列在体记录小鼠背侧海马神经元的放电活动。根据神经元的峰电位发放频率和峰电位谷-峰波宽鉴定出中间神经元(
n
=105)
并分析其在训练期间和训练后慢波睡眠期间的放电活动变化。
结果
2
① 在CR习得训练早期(第1、2天)
CS能够诱发背侧海马中间神经元出现显著增强的发放活动(
P
<
0.05);训练后慢波睡眠期间尖波涟漪波(sharp wave ripple
SWR)振荡发生时
配对组小鼠背侧海马中间神经元发放频率显著低于假配对组(
P
<
0.05)。②在CR习得训练后期(第3、4天)
与假配对组比较
配对组CS诱发的背侧海马中间神经元放电活动增强不明显; 2组小鼠背侧海马中间神经元在训练后慢波睡眠期SWR振荡发生时的发放频率差异无统计学意义。
结论
2
背侧海马中间神经元在联合型记忆的习得和巩固阶段会展现出不同的放电变化。
Objective
2
To investigate the changes and features of firing activities of interneurons in dorsal hippocampus during the acquisition and consolidation of associative memory.
Methods
2
Trace eyeblink conditioning (tEBC) was utilized as a behavioral model of associative memory.A total of 18 wild-type C57BL/6 mice (male
10~12 weeks old
weighing 22~25 g) were randomly divided into a paired group (
n
=9) and an unpaired group (
n
=9).Paired presentations of conditioned stimulus (CS) and unconditioned stimulus (US) were utilized to train these mice.The mice from the paired group were given US training in 250 ms after CS training
and those from the unpaired group received similar doses of CS and US trainin
g
but with no paired relationship in time.After 4 consecutive days'training
the mice of the paired group acquired tEBC
manifesting conditioned eyeblink responses (CR).Tetrode arrays were applied to record neuronal activity in dorsal hippocampus during both tEBC training epoch and the 1.5 h epoch after training.The putative interneurons (
n
=105) were identified according to their firing rate and spike width from trough to peak.Specific changes in hippocampal interneurons activity during tEBC training and post-training slow wave sleep were analyzed respectively.
Results
2
① At the early stage of CR acquisition (the 1
st
and 2
nd
days)
CS could evoke significantly greater activity of dorsal hippocampal interneurons in the paired group (
P
<
0.05).During sharp wave ripples (SWR) in the post-training slow wave sleep
the firing rate of dorsal hippocampal interneurons was significantly lower in the paired group than the unpaired group (
P
<
0.05).②At the late stage of CR acquisition (the 3
rd
and 4
th
days)
no significant differences in CS evoked activity of dorsal hippocampal interneurons were observed between the paired group and unpaired group
neither in the firing rate of dorsal hippocampal interneurons during SWR in the post-training slow wave sleep between the 2 groups.
Conclusion
2
The dorsal hippocampal interneurons show opposite changes in firing activity during the acquisition and consolidation of associative memory.
GIOVANNIELLO J, BRAVO-RIVERA C, ROSENKRANZ A, et al . Stress, associative learning, and decision-making[J ] . Neurobiol Learn Mem, 2023, 204: 107812. DOI: 10.1016/j.nlm.2023.107812.
STEINKRAUSS A C, CARPENTER C M, TARKENTON M K, et al . Neural distinctiveness and discriminability underlying unitization and associative memory in aging[J ] . Aging Brain, 2023, 4: 100097. DOI: 10.1016/j.nbas.2023.100097.
HALVERSON H E, KIM J, FREEMAN J H. Dynamic changes in local activity and network interactions among the anterior cingulate, amygdala, and cerebellum during associative learning[J]. J Neurosci, 2023, 43(49): 8385-8402. DOI: 10.1523/JNEUROSCI.0731-23.2023.
PILKIW M, TAKEHARA-NISHIUCHI K. Neural representations of time-linked memory[J]. Neurobiol Learn Mem, 2018, 153(Pt A): 57-70. DOI: 10.1016/j.nlm.2018.03.024.
WEISS C, KRONFORST-COLLINS M A, DISTERHOFT J F. Activity of hippocampal pyramidal neurons during trace eyeblink conditioning[J]. Hippocampus, 1996, 6(2): 192-209. DOI: 10.1002/(SICI)1098-1063(1996)6: 2<192: :AID-HIPO9>3.0.CO;2-R.
LI RR, YAN J, CHEN H, et al . Sleep deprivation impairs learning-induced increase in hippocampal sharp wave ripples and associated spike dynamics during recovery sleep[J ] . Cereb Cortex, 2022, 32(4): 824-838. DOI: 10.1093/cercor/bhab247.
ROUMIS D K, FRANK L M. Hippocampal sharp-wave ripples in waking and sleeping states[J]. Curr Opin Neurobiol, 2015, 35: 6-12. DOI: 10.1016/j.conb.2015.05.001.
MOUNT R A, SRIDHAR S, HANSEN K R, et al . Distinct neuronal populations contri bute to trace conditioning and extinction learning in the hippocampal CA1[J ] . eLife, 2021, 10: e56491. DOI: 10.7554/eLife.56491.
PELKEY K A, CHITTAJALLU R, CRAIG M T, et al . Hippocampal GABAergic inhibitory interneurons[J ] . Physiol Rev, 2017, 97(4): 1619-1747. DOI: 10.1152/physrev.00007.2017.
TZILIVAKI A, TUKKER J J, MAIER N, et al . Hippocampal GABAergic interneurons and memory[J ] . Neuron, 2023, 111(20): 3154-3175. DOI: 10.1016/j.neuron.2023.06.016.
MCKAY B M, OH M M, DISTERHOFT J F. Learning increases intrinsic excitability of hippocampal interneurons[J]. J Neurosci, 2013, 33(13): 5499-5506. DOI: 10.1523/JNEUROSCI.4068-12.2013.
LOVETT-BARRON M, KAIFOSH P, KHEIRBEK M A, et al . Dendritic inhibition in the hippocampus supports fear learning[J ] . Science, 2014, 343(6173): 857-863. DOI: 10.1126/science.1247485.
ZHANG W W, LI R R, ZHANG J, et al . Hippocampal interneurons are required for trace eyeblink conditioning in mice[J ] . Neurosci Bull, 2021, 37(8): 1147-1159. DOI: 10.1007/s12264-021-00700-0.
HE X Z, LI J R, ZHOU G J, et al . Gating of hippocampal rhythms and memory by synaptic plasticity in inhibitory interneurons[J ] . Neuron, 2021, 109(6): 1013-1028. e9. DOI: 10.1016/j.neuron.2021.01.014.
GRUART A, SANCHEZ-CAMPUSANO R, FERNANDEZ-GUIZAN A, et al . A differential and timed contribution of identified hippocampal synapses to associative learning in mice[J ] . Cereb Cortex, 2015, 25(9): 2542-2555. DOI: 10.1093/cercor/bhu054.
ANDERSON E B, GROSSRUBATSCHER I, FRANK L. Dynamic hippocampal circuits support learning- and memory-guided behaviors[J]. Cold Spring Harb Symp Quant Biol, 2014, 79: 51-58. DOI: 10.1101/sqb.2014.79.024760.
ZHANG J, ZHANG K Y, ZHANG L B, et al . A method for combining multiple-units readout of optogenetic control with natural stimulation-evoked eyeblink conditioning in freely-moving mice[J ] . Sci Rep, 2019, 9(1): 1857. DOI: 10.1038/s41598-018-37885-w.
王斌, 胡昱博, 童柳霞, 等. 腹内侧丘脑神经元在小鼠觉醒-睡眠周期中的放电特征及变化[J]. 陆军军医大学学报, 2022, 44(16): 1585-1591. DOI: 10.16016/j.2097-0927.202202028.
WANG B, HU Y B, TONG L X, et al . Characteristics of ve ntromedial thalamic neuronal activity during sleep-wake cycle in mice[J ] . J Army Med Univ, 2022, 44(16): 1585-1591. DOI: 10.16016/j.2097-0927.202202028.
WEISS C, DISTERHOFT J F. The impact of hippocampal lesions on trace-eyeblink conditioning and forebrain-cerebellar interactions[J]. Behav Neurosci, 2015, 129(4): 512-522. DOI: 10.1037/bne0000061.
TAKEHARA K, KAWAHARA S, KIRINO Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning[J]. J Neurosci, 2003, 23(30): 9897-9905. DOI: 10.1523/JNEUROSCI.23-30-09897.2003.
GREEN J T, ARENOS J D. Hippocampal and cerebellar single-unit activity during delay and trace eyeblink conditioning in the rat[J]. Neurobiol Learn Mem, 2007, 87(2): 269-284. DOI: 10.1016/j.nlm.2006.08.014.
LI R R, ZHANG W W, ZHANG J, et al . Sustained activity of hippocampal parvalbumin-expressing interneurons supports trace eyeblink conditioning in mice[J ] . J Neurosci, 2022, 42(44): 8343-8360. DOI: 10.1523/JNEUROSCI.0834-22.2022.
MCKENZIE S. Inhibition shapes the organization of hippocampal representations[J]. Hippocampus, 2018, 28(9): 659-671. DOI: 10.1002/hipo.22803.
DE ZEEUW C I, CANTO C B. Sleep deprivation directly following eyeblink-conditioning impairs memory consolidation[J]. Neurobiol Learn Mem, 2020, 170: 107165. DOI: 10.1016/j.nlm.2020.107165.
JOO H R, FRANK L M. The hippocampal sharp wave-ripple in memory retrieval for immediate use and consolidation[J]. Nat RevNeurosci, 2018, 19(12): 744-757. DOI: 10.1038/s41583-018-0077-1.
EVANGELISTA R, CANO G, COOPER C, et al . Generation of sharp wave-ripple events by disinhibition[J ] . J Neurosci, 2020, 40(41): 7811-7836. DOI: 10.1523/JNEUROSCI.2174-19.2020.
HUELIN GORRIZ M, TAKIGAWA M, BENDOR D. The role of experience in prioritizing hippocampal replay[J]. Nat Commun, 2023, 14(1): 8157. DOI: 10.1038/s41467-023-43939-z.
OGNJANOVSKI N, SCHAEFFER S, WU J X, et al . Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation[J ] . Nat Commun, 2017, 8: 15039. DOI: 10.1038/ncomms15039.
XIA F, RICHARDS B A, TRAN M M, et al . Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation[J ] . eLife, 2017, 6: e27868. DOI: 10.7554/eLife.27868.
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