Understanding hippocampal activity by using purposeful behavior: Place navigation induces place cell discharge in both task-relevant and task-irrelevant spatial reference frames

Zinyuk, L.

doi:10.1073/pnas.050576397

Cited by 59 publications

(43 citation statements)

References 14 publications

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“…Although conclusive evidence has demonstrated that the hippocampal representations of space can be dissociated into separate frames of reference (Gothard et al, 1996a,b; Zinyuk et al, 2000; Knierim, 2002; Lee et al, 2004), these dissociations do not necessarily entail distinct mechanisms of the formation of spatial firing. Rivard et al (2004) showed evidence that there were at least two classes of place cells, one class that signals proximity to a barrier and another that signals location in an allocentric reference frame.…”

Section: Discussionmentioning

confidence: 99%

Influence of local objects on hippocampal representations: Landmark vectors and memory

2013

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The hippocampus is thought to represent nonspatial information in the context of spatial information. An animal can derive both spatial information as well as nonspatial information from the objects (landmarks) it encounters as it moves around in an environment. Here, we demonstrate correlates of both object-derived spatial as well as nonspatial information in the hippocampus of rats foraging in the presence of objects. We describe a new form of CA1 place cells, called landmark-vector cells, that encode spatial locations as a vector relationship to local landmarks. Such landmark vector relationships can be dynamically encoded. Of the 26 CA1 neurons that developed new fields in the course of a day’s recording sessions, in 8 cases the new fields were located at a similar distance and direction from a landmark as the initial field was located relative to a different landmark. We also demonstrate object-location memory in the hippocampus. When objects were removed from an environment or moved to new locations, a small number of neurons in CA1 and CA3 increased firing at the locations where the objects used to be. In some neurons, this increase occurred only in one location, indicating object +place conjunctive memory; in other neurons the increase in firing was seen at multiple locations where an object used to be. Taken together, these results demonstrate that the spatially restricted firing of hippocampal neurons encode multiple types of information regarding the relationship between an animal’s location and the location of objects in its environment.

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Section: Discussionmentioning

confidence: 99%

Influence of local objects on hippocampal representations: Landmark vectors and memory

2013

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“…Epoch remapping may represent a mechanism by which the hippocampus is able to distinguish distinct events that occur in the same location, a critical component of episodic memory (Tulving, 1972). Observing three separate remapping patterns (no remapping, epoch remapping and task remapping) within the same population of neurons is an example of partial remapping, in which manipulations of the recording environment reveal subpopulations of place cells that are tied to separate reference frames (Gothard et al, 1996; Shapiro et al, 1997; Tanila et al, 1997; Skaggs and McNaugton, 1998; Zinyuk et al, 2000; Knierim, 2002; Anderson and Jeffery, 2003; Paz-Villagran et al, 2004). The partial remapping observed between the three behavioral epochs indicates that the epoch-unique place field representations occur in conjunction with a stable spatial code (place fields that did not remap between epochs), and task code (task remapping place fields).…”

Section: Discussionmentioning

confidence: 99%

Dynamic coding of dorsal hippocampal neurons between tasks that differ in structure and memory demand

Hallock

Griffin

2012

Hippocampus

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Hippocampal place fields show remapping between environments that contain sufficiently different contextual features, a phenomenon that may reflect a mechanism for episodic memory formation. Previous studies have shown that place fields remap to changes in the configuration of visual landmarks in an environment. Other experiments have demonstrated that remapping can occur with experience, even when the visual features of an environment remain stable. A special case of remapping may be trajectory coding, the tendency for hippocampal neurons to exhibit different firing rates depending upon recently visited or upcoming spatial locations. To further delineate the conditions under which different task features elicit remapping, we recorded from place cells in dorsal CA1 of hippocampus while rats switched between tasks that differed in memory demand and task structure; continuous spatial alternation (CA), delayed spatial alternation (DA), and tactile-visual conditional discrimination (CD). Individual hippocampal neurons and populations of simultaneously recorded neurons showed coherent remapping between CA and CD. However, task remapping was rarely seen between DA and CD. Analysis of individual units revealed that even though the population retained a coherent representation of task structure across the DA and CD tasks, the majority of individual neurons consistently remapped at some point during recording sessions. In contrast with previous studies, trajectory coding on the stem of the T-maze was virtually absent during all of the tasks, suggesting that experience with multiple tasks in the same environment reduces the likelihood that hippocampal neurons will represent distinct trajectories. Trajectory coding was, however, observed during the delay period of DA. Whether place fields change in response to task or trial type or remain stable within the same environment may depend on which aspects of the context are most salient or relevant to behavior.

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“…We have used the active place avoidance paradigm to investigate cognitive information processing (Fenton et al, 1998; Zinyuk et al, 2000; Kelemen and Fenton, 2010; Kelemen and Fenton, 2013). Place information in hippocampal electrical activity toggles between the distinct stationary and rotating spatial frames during active place avoidance, indicating neural coordination (Kelemen and Fenton, 2010; Kelemen and Fenton, 2013).…”

Section: Methodsmentioning

confidence: 99%

Impaired cognitive discrimination and discoordination of coupled theta–gamma oscillations in Fmr1 knockout mice

Radwan

Dvořák

Fenton

2016

Neurobiology of Disease

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Fragile X syndrome (FXS) patients do not make the fragile X mental retardation protein (FMRP). Absence of FMRP causes dysregulated translation, abnormal synaptic plasticity and the most common form of inherited intellectual disability. But FMRP loss has minimal effects on memory itself, making it difficult to understand why absence of FMRP impairs memory discrimination and increases risk of autistic symptoms in patients, such as exaggerated responses to environmental changes. While Fmr1 knockout (KO) and wild-type (WT) mice perform cognitive discrimination tasks, we find abnormal patterns of coupling between theta and gamma oscillations in perisomatic and dendritic hippocampal CA1 local field potentials of the KO. Perisomatic CA1 theta-gamma phase-amplitude coupling (PAC) decreases with familiarity in both the WT and KO, but activating an invisible shock zone, subsequently changing its location, or turning it off, changes the pattern of oscillatory events in the LFPs recorded along the somato-dendritic axis of CA1. The cognition-dependent changes of this pattern of neural activity are relatively constrained in WT mice compared to KO mice, which exhibit abnormally weak changes during the cognitive challenge caused by changing the location of the shock zone and exaggerated patterns of change when the shock zone is turned off. Such pathophysiology might explain how dysregulated translation leads to intellectual disability in FXS. These findings demonstrate major functional abnormalities after the loss of FMRP in the dynamics of neural oscillations and that these impairments would be difficult to detect by steady-state measurements with the subject at rest or in steady conditions.

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Understanding hippocampal activity by using purposeful behavior: Place navigation induces place cell discharge in both task-relevant and task-irrelevant spatial reference frames

Cited by 59 publications

References 14 publications

Influence of local objects on hippocampal representations: Landmark vectors and memory

Influence of local objects on hippocampal representations: Landmark vectors and memory

Dynamic coding of dorsal hippocampal neurons between tasks that differ in structure and memory demand

Impaired cognitive discrimination and discoordination of coupled theta–gamma oscillations in Fmr1 knockout mice

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