scholarly journals Dentate granule cells encode auditory decisions after reinforcement learning in rats

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jia Shen ◽  
Pan-Tong Yao ◽  
Shaoyu Ge ◽  
Qiaojie Xiong

AbstractAuditory-cued goal-oriented behaviors requires the participation of cortical and subcortical brain areas, but how neural circuits associate sensory-based decisions with goal locations through learning remains poorly understood. The hippocampus is critical for spatial coding, suggesting its possible involvement in transforming sensory inputs to the goal-oriented decisions. Here, we developed an auditory discrimination task in which rats learned to navigate to goal locations based on the frequencies of auditory stimuli. Using in vivo calcium imaging in freely behaving rats over the course of learning, we found that dentate granule cells became more active, spatially tuned, and responsive to task-related variables as learning progressed. Furthermore, only after task learning, the activity of dentate granule cell ensembles represented the navigation path and predicts auditory decisions as early as when rats began to approach the goals. Finally, chemogenetic silencing of dentate gyrus suppressed task learning. Our results demonstrate that dentate granule cells gain task-relevant firing pattern through reinforcement learning and could be a potential link of sensory decisions to spatial navigation.

PLoS ONE ◽  
2017 ◽  
Vol 12 (7) ◽  
pp. e0180452 ◽  
Author(s):  
Yuichiro Hayashi ◽  
Satoshi Yawata ◽  
Kazuo Funabiki ◽  
Takatoshi Hikida

2011 ◽  
Vol 31 (11) ◽  
pp. 4345-4354 ◽  
Author(s):  
B. W. Luikart ◽  
E. Schnell ◽  
E. K. Washburn ◽  
A. L. Bensen ◽  
K. R. Tovar ◽  
...  

2016 ◽  
Vol 19 (6) ◽  
pp. 788-791 ◽  
Author(s):  
J Tiago Gonçalves ◽  
Cooper W Bloyd ◽  
Matthew Shtrahman ◽  
Stephen T Johnston ◽  
Simon T Schafer ◽  
...  

Development ◽  
2002 ◽  
Vol 129 (18) ◽  
pp. 4249-4260 ◽  
Author(s):  
Anil Bagri ◽  
Theresa Gurney ◽  
Xiaoping He ◽  
Yong-Rui Zou ◽  
Dan R. Littman ◽  
...  

The dentate gyrus is the primary afferent pathway into the hippocampus, but there is little information concerning the molecular influences that govern its formation. In particular, the control of migration and cell positioning of dentate granule cells is not clear. We have characterized more fully the timing and route of granule cell migration during embryogenesis using in utero retroviral injections. Using this information, we developed an in vitro assay that faithfully recapitulates important events in dentate gyrus morphogenesis. In searching for candidate ligands that may regulate dentate granule cell migration, we found that SDF1, a chemokine that regulates cerebellar and leukocyte migration, and its receptor CXCR4 are expressed in patterns that suggest a role in dentate granule cell migration. Furthermore, CXCR4 mutant mice have a defect in granule cell position. Ectopic expression of SDF1 in our explant assay showed that it directly regulates dentate granule cell migration. Our study shows that a chemokine is necessary for the normal development of the dentate gyrus, a forebrain structure crucial for learning and memory.


1990 ◽  
Vol 509 (1) ◽  
pp. 91-98 ◽  
Author(s):  
M.D. Mun˜oz ◽  
A. Nún˜ez ◽  
E. García-Austt

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Haruna Tamano ◽  
Naoya Oneta ◽  
Aoi Shioya ◽  
Paul A. Adlard ◽  
Ashley I. Bush ◽  
...  

2021 ◽  
Author(s):  
Hannah Twarkowski ◽  
Victor Steininger ◽  
Min Jae Kim ◽  
Amar Sahay

Memories encoded in the dentate gyrus (DG)-CA3 circuit of the hippocampus are routed from CA1 to anterior cingulate cortex (ACC) for consolidation. Although CA1 parvalbumin inhibitory neurons (PV INs) orchestrate hippocampal-cortical communication, we know less about CA3 PV INs or DG-CA3 principal neuron-IN circuit mechanisms that contribute to evolution of hippocampal-cortical ensembles during memory consolidation. Using viral genetics to selectively enhance dentate granule cell recruitment of CA3 PV INs and feed-forward inhibition (FFI) in CA3 and longitudinal in vivo calcium imaging, we demonstrate that FFI facilitates formation and maintenance of context-associated neuronal ensembles in CA1. Increasing FFI in DG-CA3 promoted context specificity of neuronal ensembles in ACC over time and enhanced long-term contextual fear memory. Our findings illuminate how FFI in DG-CA3 dictates evolution of ensemble properties in CA1 and ACC during memory consolidation and suggest a teacher-like function for hippocampal CA1 in stabilization and re-organization of cortical representations.


1998 ◽  
Vol 80 (6) ◽  
pp. 2860-2869 ◽  
Author(s):  
T. M. Gao ◽  
E. M. Howard ◽  
Z. C. Xu

Gao, T. M., E. M. Howard, and Z. C. Xu. Transient neurophysiological changes in CA3 neurons and dentate granule cells after severe forebrain ischemia in vivo. J. Neurophysiol. 80: 2860–2869, 1998. The spontaneous activities, evoked synaptic responses, and membrane properties of CA3 pyramidal neurons and dentate granule cells in rat hippocampus were compared before ischemia and ≤7 days after reperfusion with intracellular recording and staining techniques in vivo. A four-vessel occlusion method was used to induce ∼14 min of ischemic depolarization. No significant change in spontaneous firing rate was observed in both cell types after reperfusion. The amplitude and slope of excitatory postsynaptic potentials (EPSPs) in CA3 neurons decreased to 50% of control values during the first 12 h reperfusion and returned to preischemic levels 24 h after reperfusion. The amplitude and slope of EPSPs in granule cells slightly decreased 24–36 h after reperfusion. The amplitude of inhibitory postsynaptic potentials in CA3 neurons transiently increased 24 h after reperfusion, whereas that in granule cells showed a transient decrease 24–36 h after reperfusion. The duration of spike width of CA3 and granule cells became longer than that of control values during the first 12 h reperfusion. The spike threshold of both cell types significantly increased 24–36 h after reperfusion, whereas the frequency of repetitive firing evoked by depolarizing current pulse was decreased during this period. No significant change in rheobase and input resistance was observed in CA3 neurons. A transient increase in rheobase and a transient decrease in input resistance were detected in granule cells 24–36 h after reperfusion. The amplitude of fast afterhyperpolarization in both cell types increased for 2 days after ischemia and returned to normal values 7 days after reperfusion. The results from this study indicate that the neuronal excitability and synaptic transmission in CA3 and granule cells are transiently suppressed after severe forebrain ischemia. The depression of synaptic transmission and neuronal excitability may provide protection for neurons after ischemic insult.


2018 ◽  
Vol 2018 ◽  
pp. 1-11 ◽  
Author(s):  
Peter Jedlicka ◽  
Julia Muellerleile ◽  
Stephan W. Schwarzacher

The hippocampal dentate gyrus plays a role in spatial learning and memory and is thought to encode differences between similar environments. The integrity of excitatory and inhibitory transmission and a fine balance between them is essential for efficient processing of information. Therefore, identification and functional characterization of crucial molecular players at excitatory and inhibitory inputs is critical for understanding the dentate gyrus function. In this minireview, we discuss recent studies unraveling molecular mechanisms of excitatory/inhibitory synaptic transmission, long-term synaptic plasticity, and dentate granule cell excitability in the hippocampus of live animals. We focus on the role of three major postsynaptic proteins localized at excitatory (neuroligin-1) and inhibitory synapses (neuroligin-2 and collybistin).In vivorecordings of field potentials have the advantage of characterizing the effects of the loss of these proteins on the input-output function of granule cells embedded in a network with intact connectivity. The lack of neuroligin-1 leads to deficient synaptic plasticity and reduced excitation but normal granule cell output, suggesting unaltered excitation-inhibition ratio. In contrast, the lack of neuroligin-2 and collybistin reduces inhibition resulting in a shift towards excitation of the dentate circuitry.


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