scholarly journals Preexisting hippocampal network dynamics constrain optogenetically induced place fields

2019 ◽  
Author(s):  
Sam McKenzie ◽  
Roman Huszár ◽  
Daniel F. English ◽  
Kanghwan Kim ◽  
Euisik Yoon ◽  
...  

SummaryNeuronal circuits face a fundamental tension between maintaining existing structure and changing to accommodate new information. Memory models often emphasize the need to encode novel patterns of neural activity imposed by “bottom-up” sensory drive. In such models, learning is achieved through synaptic alterations, a process which potentially interferes with previously stored knowledge 1-3. Alternatively, neuronal circuits generate and maintain a preconfigured stable dynamic, sometimes referred to as an attractor, manifold, or schema 4-7, with a large reservoir of patterns available for matching with novel experiences 8-13. Here, we show that incorporation of arbitrary signals is constrained by pre-existing circuit dynamics. We optogenetically stimulated small groups of hippocampal neurons as mice traversed a chosen segment of a linear track, mimicking the emergence of place fields 1,14,15, while simultaneously recording the activity of stimulated and non-stimulated neighboring cells. Stimulation of principal neurons in CA1, but less so CA3 or the dentate gyrus, induced persistent place field remapping. Novel place fields emerged in both stimulated and non-stimulated neurons, which could be predicted from sporadic firing in the new place field location and the temporal relationship to peer neurons prior to the optogenetic perturbation. Circuit modification was reflected by altered spike transmission between connected pyramidal cell – inhibitory interneuron pairs, which persisted during post-experience sleep. We hypothesize that optogenetic perturbation unmasked sub-threshold, pre-existing place fields16,17. Plasticity in recurrent/lateral inhibition may drive learning through rapid exploration of existing states.

1997 ◽  
Vol 78 (2) ◽  
pp. 597-613 ◽  
Author(s):  
Tsuneyuki Kobayashi ◽  
Hisao Nishijo ◽  
Masaji Fukuda ◽  
Jan Bures ◽  
Taketoshi Ono

Kobayashi, Tsuneyuki, Hisao Nishijo, Masaji Fukuda, Jan Bures, and Taketoshi Ono. Task-dependent representations in rat hippocampal place neurons. J. Neurophysiol. 78: 597–613, 1997. It is suggested that the hippocampal formation is essential to spatial representations by flexible encoding of diverse information during navigation, which includes not only externally generated sensory information such as visual and auditory sensation but also ideothetic information concerning locomotion (i.e., internally generated information such as proprioceptive and vestibular sensation) as well as information concerning reward. In the present study, we investigated how various types of information are represented in the hippocampal formation, by recording hippocampal complex-spike cells from rats that performed three types of place learning tasks in a circular open field with the use of intracranial self-stimulation as reward. The intracranial self-stimulation reward was delivered in the following three contexts: if the rat 1) entered an experimenter-determined reward place within the open field, and this place was randomly varied in sequential trials; 2) entered two specific places, one within and one outside the place field (an area identified by change in activity of a place neuron); or 3) entered an experimenter-specified place outside the place field. Because the behavioral trails during navigation were more constant in the second task than in the first task, ideothetic information concerning locomotion was more relevant to acquiring reward in the second task than in the first task. Of 43 complex-spike cells recorded, 37 displayed place fields under the first task. Of these 37 place neurons, 34 also had significant reward correlates only inside the place field. Although reward and place correlates of the place neuron activity did not change between the first and second tasks, neuronal correlates to behavioral variables for locomotion such as movement speed, direction, and turning angle significantly increased in the second task. Furthermore, 6 of 31 place neurons tested with the third task, in which the reward place was located outside the original place field, shifted place fields. The results indicated that neuronal correlates of most place neurons flexibly increased their sensitivity to relevant information in a given context and environment, and some place neurons changed the place field per se with place reward association. These results suggest two strategies for how hippocampal neurons incorporate an incredible variety of perceptions into a unified representation of the environment: through flexible use of information and the creation of new representations.


2001 ◽  
Vol 85 (1) ◽  
pp. 105-116 ◽  
Author(s):  
James J. Knierim ◽  
Bruce L. McNaughton

“Place” cells of the rat hippocampus are coupled to “head direction” cells of the thalamus and limbic cortex. Head direction cells are sensitive to head direction in the horizontal plane only, which leads to the question of whether place cells similarly encode locations in the horizontal plane only, ignoring the z axis, or whether they encode locations in three dimensions. This question was addressed by recording from ensembles of CA1 pyramidal cells while rats traversed a rectangular track that could be tilted and rotated to different three-dimensional orientations. Cells were analyzed to determine whether their firing was bound to the external, three-dimensional cues of the environment, to the two-dimensional rectangular surface, or to some combination of these cues. Tilting the track 45° generally provoked a partial remapping of the rectangular surface in that some cells maintained their place fields, whereas other cells either gained new place fields, lost existing fields, or changed their firing locations arbitrarily. When the tilted track was rotated relative to the distal landmarks, most place fields remapped, but a number of cells maintained the same place field relative to the x-y coordinate frame of the laboratory, ignoring the z axis. No more cells were bound to the local reference frame of the recording apparatus than would be predicted by chance. The partial remapping demonstrated that the place cell system was sensitive to the three-dimensional manipulations of the recording apparatus. Nonetheless the results were not consistent with an explicit three-dimensional tuning of individual hippocampal neurons nor were they consistent with a model in which different sets of cells are tightly coupled to different sets of environmental cues. The results are most consistent with the statement that hippocampal neurons can change their “tuning functions” in arbitrary ways when features of the sensory input or behavioral context are altered. Understanding the rules that govern the remapping phenomenon holds promise for deciphering the neural circuitry underlying hippocampal function.


2020 ◽  
Author(s):  
Wei Guo ◽  
Jie J. Zhang ◽  
Jonathan P. Newman ◽  
Matthew A. Wilson

AbstractLatent learning allows the brain the transform experiences into cognitive maps, a form of implicit memory, without reinforced training. Its mechanism is unclear. We tracked the internal states of the hippocampal neural ensembles and discovered that during latent learning of a spatial map, the state space evolved into a low-dimensional manifold that topologically resembled the physical environment. This process requires repeated experiences and sleep in-between. Further investigations revealed that a subset of hippocampal neurons, instead of rapidly forming place fields in a novel environment, remained weakly tuned but gradually developed correlated activity with other neurons. These ‘weakly spatial’ neurons bond activity of neurons with stronger spatial tuning, linking discrete place fields into a map that supports flexible navigation.


Hippocampus ◽  
2016 ◽  
Vol 26 (10) ◽  
pp. 1328-1344 ◽  
Author(s):  
W.K.L. Witharana ◽  
J. Cardiff ◽  
M.K. Chawla ◽  
J.Y. Xie ◽  
C.B. Alme ◽  
...  

2017 ◽  
Vol 37 (49) ◽  
pp. 12031-12049 ◽  
Author(s):  
Hsin-Yi Kao ◽  
Dino Dvořák ◽  
EunHye Park ◽  
Jana Kenney ◽  
Eduard Kelemen ◽  
...  

2019 ◽  
Author(s):  
Adrian Aleman-Zapata ◽  
Richard GM Morris ◽  
Lisa Genzel

AbstractMemory reactivation during NonREM-ripples is thought to communicate new information to a systems-wide network. Cortical high frequency events have also been described that co-occur with ripples. Focusing on NonREM sleep after different behaviors, both hippocampal ripples and parietal high frequency oscillations were detected. A bimodal frequency distribution was observed in the parietal high frequency events, faster and slower, with increases in prefrontal directionality measured by Granger causality analysis specifically seen during the fast parietal oscillations. Furthermore, fast events activated prefrontal-parietal cortex whereas slow events activated hippocampal-parietal areas. Finally, there was a learning-induced increase in both number and size of fast high frequency events. These patterns were not seen after novelty exposure or foraging, but occurred after the learning of a new goal location in a maze. Disruption of either sleep or hippocampal ripples impaired long-term memory consistent with these having a role in memory consolidation.


Author(s):  
Soledade Paiva de Sousa ◽  
Miguel Baptista-Bastos

During the first year’s teaching on the architecture course at FAUTL (Lisbon), a number of questions have arisen concerning architectural project learning, related to theoretical studies of assimilation and retention.In most of this year’s students, the existing structure of their knowledge is noticeably inhibiting the assimilation of new data, so making the professor’s role in the process very difficult.At present, learning is not conscious, being influenced by several factors, both external to and inherent in, changes within education. A clear transformation of the cognitive structure has not been observed, with the result that new information is not being assimilated by the majority of students.It is recommended that, concurrent with the general programme, students do and repeat certain exercises until the course contents are thoroughly incorporated and articulated with previous concepts: it is intended that such an approach will enable the conscious and rational retention of material.In this process, the professor reviews the knowledge acquired by the students while also establishing that they already have some information about what they are learning.Therefore, more repetition is suggested in the practice of the architectural project planning component over the semesters, moving away from the internalisation of knowledge through “meaningful learning”, (D. P. Ausubel)


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Aaron D Milstein ◽  
Yiding Li ◽  
Katie C Bittner ◽  
Christine Grienberger ◽  
Ivan Soltesz ◽  
...  

Learning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neurons. Here we found that this behavioral timescale synaptic plasticity (BTSP) can also reshape existing place fields via bidirectional synaptic weight changes that depend on the temporal proximity of plateau potentials to pre-existing place fields. When evoked near an existing place field, plateau potentials induced less synaptic potentiation and more depression, suggesting BTSP might depend inversely on postsynaptic activation. However, manipulations of place cell membrane potential and computational modeling indicated that this anti-correlation actually results from a dependence on current synaptic weight such that weak inputs potentiate and strong inputs depress. A network model implementing this bidirectional synaptic learning rule suggested that BTSP enables population activity, rather than pairwise neuronal correlations, to drive neural adaptations to experience.


2020 ◽  
Author(s):  
EB Knudsen ◽  
JD Wallis

AbstractThe hippocampus is thought to encode a ‘cognitive map’, a structural organization of knowledge about relationships in the world. Place cells, spatially selective hippocampal neurons that have been extensively studied in rodents, are one component of this map, describing the relative position of environmental features. However, whether this map extends to abstract, cognitive information remains unknown. Using the relative reward value of cues to define continuous ‘paths’ through an abstract value space, we show that single neurons in primate hippocampus encode this space through value place fields, much like a rodent’s place neurons encode paths through physical space. Value place fields remapped when cues changed, but also became increasingly correlated across contexts, allowing maps to become generalized. Our findings help explain the critical contribution of the hippocampus to value-based decision-making, providing a mechanism by which knowledge of relationships in the world can be incorporated into reward predictions for guiding decisions.


2019 ◽  
Author(s):  
Donovan M Ashby ◽  
Jeremy K Seamans ◽  
Yu Tian Wang

AbstractSynaptic plasticity mechanisms may help shape hippocampal place field representations of novel environments, yet direct evidence for how this occurs is lacking. Using multi-channel recordings in freely moving rats, we demonstrate that novelty exploration results in widespread de novo long-term depression (LTD) at hippocampal CA1 synapses in a pathway-specific manner, while blockade of LTD expression impairs the maintenance of newly formed place fields. This study therefore reveals an unrecognized role for LTD in the formation and maintenance of hippocampal place fields in novel environments.


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