scholarly journals Prefrontal cortical activity predicts the occurrence of nonlocal hippocampal representations during spatial navigation

PLoS Biology ◽  
2021 ◽  
Vol 19 (9) ◽  
pp. e3001393
Author(s):  
Jai Y. Yu ◽  
Loren M. Frank

The receptive field of a neuron describes the regions of a stimulus space where the neuron is consistently active. Sparse spiking outside of the receptive field is often considered to be noise, rather than a reflection of information processing. Whether this characterization is accurate remains unclear. We therefore contrasted the sparse, temporally isolated spiking of hippocampal CA1 place cells to the consistent, temporally adjacent spiking seen within their spatial receptive fields (“place fields”). We found that isolated spikes, which occur during locomotion, are strongly phase coupled to hippocampal theta oscillations and transiently express coherent nonlocal spatial representations. Further, prefrontal cortical activity is coordinated with and can predict the occurrence of future isolated spiking events. Rather than local noise within the hippocampus, sparse, isolated place cell spiking reflects a coordinated cortical–hippocampal process consistent with the generation of nonlocal scenario representations during active navigation.

2020 ◽  
Author(s):  
Jai Y. Yu ◽  
Loren M. Frank

AbstractThe receptive field of a neuron describes the regions of a stimulus space where the neuron is consistently active. Sparse spiking outside of the receptive field is often considered to be noise, rather than a reflection of information processing. Whether this characterization is accurate remains unclear. We therefore contrasted the sparse, temporally isolated spiking of hippocampal CA1 place cells to the consistent, temporally adjacent spiking seen within their spatial receptive fields (“place fields”). We found that isolated spikes, which occur during locomotion, are more strongly phase coupled to hippocampal theta oscillations than adjacent spikes and, surprisingly, transiently express coherent representations of non-local spatial representations. Further, prefrontal cortical activity is coordinated with, and can predict the occurrence of future isolated spiking events. Rather than local noise within the hippocampus, sparse, isolated place cell spiking reflects a coordinated cortical-hippocampal process consistent with the generation of non-local scenario representations during active navigation.


Science ◽  
2020 ◽  
Vol 370 (6513) ◽  
pp. 247-250 ◽  
Author(s):  
Mengni Wang ◽  
David J. Foster ◽  
Brad E. Pfeiffer

Neural networks display the ability to transform forward-ordered activity patterns into reverse-ordered, retrospective sequences. The mechanisms underlying this transformation remain unknown. We discovered that, during active navigation, rat hippocampal CA1 place cell ensembles are inherently organized to produce independent forward- and reverse-ordered sequences within individual theta oscillations. This finding may provide a circuit-level basis for retrospective evaluation and storage during ongoing behavior. Theta phase procession arose in a minority of place cells, many of which displayed two preferred firing phases in theta oscillations and preferentially participated in reverse replay during subsequent rest. These findings reveal an unexpected aspect of theta-based hippocampal encoding and provide a biological mechanism to support the expression of reverse-ordered sequences.


2019 ◽  
Author(s):  
Julien Fournier ◽  
Aman B Saleem ◽  
E Mika Diamanti ◽  
Miles J Wells ◽  
Kenneth D Harris ◽  
...  

Neurons in primary visual cortex (V1) are influenced by the animal’s position in the environment and encode positions that correlate with those encoded by hippocampus (CA1). Might V1’s encoding of spatial positions be inherited from hippocampal regions? If so, it should depend on non-visual factors that affect the encoding of position in hippocampus, such as the physical distance traveled and the phase of theta oscillations. We recorded V1 and CA1 neurons while mice ran through a virtual corridor and confirmed these predictions. Spatial representations in V1 and CA1 were correlated even in the absence of visual cues. Moreover, similar to CA1 place cells, the spatial responses of V1 neurons were influenced by the physical distance traveled and the phase of hippocampal theta oscillations. These results reveal a modulation of cortical sensory processing by non-sensory estimates of position that might originate in hippocampal regions.


2018 ◽  
Author(s):  
Anirvan M. Sengupta ◽  
Mariano Tepper ◽  
Cengiz Pehlevan ◽  
Alexander Genkin ◽  
Dmitri B. Chklovskii

AbstractMany neurons in the brain, such as place cells in the rodent hippocampus, have localized receptive fields, i.e., they respond to a small neighborhood of stimulus space. What is the functional significance of such representations and how can they arise? Here, we propose that localized receptive fields emerge in similarity-preserving networks of rectifying neurons that learn low-dimensional manifolds populated by sensory inputs. Numerical simulations of such networks on standard datasets yield manifold-tiling localized receptive fields. More generally, we show analytically that, for data lying on symmetric manifolds, optimal solutions of objectives, from which similarity-preserving networks are derived, have localized receptive fields. Therefore, nonnegative similarity-preserving mapping (NSM) implemented by neural networks can model representations of continuous manifolds in the brain.


2021 ◽  
Author(s):  
Eloy Parra-Barrero ◽  
Kamran Diba ◽  
Sen Cheng

AbstractNavigation through space involves learning and representing relationships between past, current and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations start behind the animal’s location and then sweep forward. However, the exact relationship between phase and represented and true positions remains unclear and even paradoxical. Here, we formalize previous notions as ‘spatial’ or ‘temporal’ sweeps, analyze single-cell and population variables in recordings from rat CA1 place cells, and compare them to model simulations. We show that neither sweep type quantitatively accounts for all relevant variables. Thus we introduce ‘behavior-dependent’ sweeps, which fit our key observation that sweep length, and hence place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. This structured heterogeneity is essential for understanding the hippocampal code.


2003 ◽  
Vol 90 (2) ◽  
pp. 822-831 ◽  
Author(s):  
James R. Müller ◽  
Andrew B. Metha ◽  
John Krauskopf ◽  
Peter Lennie

We examined in anesthetized macaque how the responses of a striate cortical neuron to patterns inside the receptive field were altered by surrounding patterns outside it. The changes in a neuron's response brought about by a surround are immediate and transient: they arise with the same latency as the response to a stimulus within the receptive field (this argues for a source locally in striate cortex) and become less effective as soon as 27 ms later. Surround signals appeared to exert their influence through divisive interaction (normalization) with those arising in the receptive field. Surrounding patterns presented at orientations slightly oblique to the preferred orientation consistently deformed orientation tuning curves of complex (but not simple) cells, repelling the preferred orientation but without decreasing the discriminability of the preferred grating and ones at slightly oblique orientations. By reducing responsivity and changing the tuning of complex cells locally in stimulus space, surrounding patterns reduce the correlations among responses of neurons to a particular stimulus, thus reducing the redundancy of image representation.


1985 ◽  
Vol 54 (1) ◽  
pp. 168-183 ◽  
Author(s):  
H. A. Swadlow ◽  
T. G. Weyand

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of LGNd neurons and optic tract axons in the awake, unparalyzed state. We found eye position to remain within a range of less than 1.0 degrees for periods of 4-5 min, and in some cases for periods in excess of 10 min. Such stability is comparable to that seen in awake monkeys that have been trained to fixate. Receptive fields of dorsal lateral geniculate nucleus (LGNd) neurons were analyzed, and approximately 84% were concentrically organized. This is a higher value than previously reported in this species. In addition, the receptive-field centers of concentric cells were much smaller than those previously reported (mean diameter = 2.5 degrees). Most remaining neurons in the LGNd were either directionally selective (6.5%) or motion/uniform (6.5%). Concentric cells were classified as sustained or transient based on response duration to standing contrast. In the LGNd the receptive fields of sustained concentric cells were predominantly near the horizontal meridian, within the representation of the visual streak, while the receptive-field positions of transient concentric cells were more prevalent in the upper visual field. In the optic tract the receptive-field positions of both sustained and transient cells were more evenly distributed than was seen in the LGNd. Sustained and transient concentric cells in LGNd showed primarily nonlinear spatial summation. The receptive-field properties of LGNd neurons were related to geniculocortical antidromic latency. Most LGNd neurons of all receptive-field classes projected axons to the visual cortex. Thus, any intrinsic interneurons in the rabbit LGNd may have receptive-field properties similar to those of some principal neurons. There was significant overlap in the distribution of antidromic latencies in neurons of different receptive-field classes. Concentric sustained neurons, however, did conduct somewhat more slowly than did concentric transient neurons. Nonvisual sensory stimuli that resulted in EEG arousal (hippocampal theta activity) had a profound effect on the response duration of most (28/32) sustained concentric neurons. For these cells, the sustained response to standing contrast began to diminish and sometimes disappeared after 2-15 s. However, arousing stimuli that resulted in hippocampal theta activity reestablished the sustained response. Such arousing stimuli usually had little or no effect on the discharge of the cell in the absence of visual stimuli. Arousing stimuli had no effect on optic tract axons with sustained concentric receptive-field properties.(ABSTRACT TRUNCATED AT 400 WORDS)


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