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.; Kubík, Štěpán; Kaminsky, Yu.; Fenton, André A.; Bureš, Jan

doi:10.1073/pnas.97.7.3771

Cited by 78 publications

(53 citation statements)

References 36 publications

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“…When the animal is put back in the environment, an unspecified recognition process decides whether the current surroundings are familiar or novel. We imagine that the decision rules are very complex and depend on the behavioral requirements in the environment as well as the immediate sensory information (Markus et al 1995; Zinyuk et al 2000). We do not consider further what happens if a new template must be built.…”

Section: Discussionmentioning

confidence: 99%

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

Fenton

Csizmadia

Muller

2000

The Journal of General Physiology

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To better understand how hippocampal place cell activity is controlled by sensory stimuli, and to further elucidate the nature of the environmental representation provided by place cells, we have made recordings in the presence of two distinct visual stimuli under standard conditions and after several manipulations of these stimuli. In line with a great deal of earlier work, we find that place cell activity is constant when repeated recordings are made in the standard conditions in which the centers of the two stimuli, a black card and a white card, are separated by 135° on the wall of a cylindrical recording chamber. Rotating the two stimuli by 45° causes equal rotations of place cell firing fields. Removing either card and rotating the other card also causes fields to rotate equally, showing that the two stimuli are individually salient. Increasing or decreasing the card separation (card reconfiguration) causes a topological distortion of the representation of the cylinder floor such that field centers move relative to each other. We also found that either kind of reconfiguration induces a position-independent decrease in the intensity of place cell firing. We argue that these results are not compatible with either of two previously stated views of the place cell representation; namely, a nonspatial theory in which each place cell is tuned to an arbitrarily selected subset of available stimuli or a rigid map theory. We propose that our results imply that the representation is map-like but not rigid; it is capable of undergoing stretches without altering the local arrangement of firing fields.

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Section: Discussionmentioning

confidence: 99%

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

Fenton

Csizmadia

Muller

2000

The Journal of General Physiology

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“…Place preference navigation (Rossier et al, 2000) training on the rotating arena increased the prevalence of room frame-specific and conjunctive room and arena frame-specific place cell discharge patterns in response to continuous rotation. Disorganized responses were reduced by navigation training, and this acquired "frame specificity" was preserved when the rats were no longer navigating (Zinyuk et al, 2000;Fenton et al, 2002), suggesting that at the level of cellular behavior, the separate representation of room and arena information is acquired during place learning on a rotating arena. Similarly, Bostock et al (1991), Lever et al (2002), and Hayman et al (2003) demonstrated that place cell remapping developed with experience, indicating neural stimulus separation is also an acquired property.…”

Section: Segregation and Representation-distinct Hippocampal Functionsmentioning

confidence: 99%

Behavioral Evidence That Segregation and Representation Are Dissociable Hippocampal Functions

Kubík¹,

Fenton²

2005

J. Neurosci.

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Hippocampal activity is thought to encode spatial representations in a distributed associative network. This idea predicts that partial hippocampal lesions would spare acquisition and impair retrieval of a place response as long as enough connections remained intact to encode associations. Water maze experiments supported the predictions, but the prediction of impaired retrieval was not supported when tetrodotoxin (TTX) was injected into one hippocampus and rats were tested in a place avoidance task on a rotating arena with shallow water. The rotation dissociated relevant distal stimuli from irrelevant self-motion stimuli. To explain the discrepancy, we hypothesized that the segregation of relevant and irrelevant stimuli and stimuli association into representations are distinct hippocampus-dependent operations, and whereas associative representation is more sensitive to disruption during retrieval than learning, stimulus segregation is more sensitive to disruption during learning than during retrieval. The following predictions were tested: (1) the TTX injection would spare learning but (2) impair retrieval of a place response in the water maze, which has a high associative representational demand but a low demand for segregation; (3) the injection would impair learning but (4) spare retrieval of place avoidance in the rotating arena filled with water, which has a high demand for stimulus segregation but a low associative representational demand. All four predictions were confirmed. The hypothesis also explains the pattern of sparing and impairment after the TTX injection in other place avoidance task variants, leading us to conclude that stimulus separation and association representation are dissociable functions of the hippocampus.

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“…They cannot use substratal idiothesis (40) or the arena-based cues that support it because the rotation makes this arena-based coordinate frame unstable with respect to the to-be-avoided sector. Nonetheless, the rats are probably aware of this arena information because the discharge of some hippocampal place cells remains organized in the arena frame during rotation despite explicitly training the rat to solve a room-frame defined allothetic place preference task (11). A key difference between the active allothetic avoidance and the standard water maze tasks is that in the dry arena, but not the water maze, there is a supply of substrate-anchored olfactory and tactile marks as well as the idiothesis they support.…”

Section: A Specific Role Of the Hippocampus In Organizing Informationmentioning

confidence: 99%

Inactivating one hippocampus impairs avoidance of a stable room-defined place during dissociation of arena cues from room cues by rotation of the arena

Cimadevilla

Wesierska

Fenton

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

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148

136

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Unilateral intrahippocampal injections of tetrodotoxin were used to temporarily inactivate one hippocampus during specific phases of training in an active allothetic place avoidance task. The rat was required to use landmarks in the room to avoid a room-defined sector of a slowly rotating circular arena. The continuous rotation dissociated room cues from arena cues and moved the arena surface through a part of the room in which foot-shock was delivered. The rat had to move away from the shock zone to prevent being transported there by the rotation. Unilateral hippocampal inactivations profoundly impaired acquisition and retrieval of the allothetic place avoidance. Posttraining unilateral hippocampal inactivation also impaired performance in subsequent sessions. This allothetic place avoidance task seems more sensitive to hippocampal disruption than the standard water maze task because the same unilateral hippocampal inactivation does not impair performance of the variable-start, fixed hidden goal task after procedural training. The results suggest that the hippocampus not only encodes allothetic relationships amongst landmarks, it also organizes perceived allothetic stimuli into systems of mutually stable coordinates. The latter function apparently requires greater hippocampal integrity.T he rodent hippocampus is a key neural system for processing information about the current spatial arrangement of stimuli and events (1-4), but it is still unclear what spatial computations the hippocampus actually does. One direction of the current experimental effort in this area is studying what aspects of spatial information the hippocampal network stores (5-12); a second is studying what spatial computations an intact hippocampal system is necessary for (13)(14)(15)(16)(17)(18)(19).It is crucial for this latter approach that there are behavioral paradigms, with clearly defined demands, that subjects must solve by using a limited set of potential solutions. The standard, variable-start, fixed hidden goal place navigation task in the water maze (20) has been invaluable because it allows the optimal solution to be readily distinguished from other less efficient strategies. The optimal strategy is for the rat to learn the allothetic relationships between distant, typically visual stimuli and the position of the escape platform. The absence of stable stimuli on the liquid substrate, like visual and tactile marks and odor cues, and the use of variable start locations make it difficult after standard training for the rat to solve the task optimally by using beacon-guided, praxis, or route-following strategies.Since the early eighties, place learning in the water maze has been used in lesion studies to elucidate the role of the hippocampus in spatial cognition (21,22). Selective bilateral lesions of the dentate gyrus and CA3-CA4 were found to severely impair water maze performance (23). However, in that study, unilateral dentate gyrus lesions, but not CA3-CA4 lesions disturbed water maze performance.One difficulty in interpreting t...

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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 78 publications

References 36 publications

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

Behavioral Evidence That Segregation and Representation Are Dissociable Hippocampal Functions

Inactivating one hippocampus impairs avoidance of a stable room-defined place during dissociation of arena cues from room cues by rotation of the arena

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