Hippocampal Place Cell Instability after Lesions of the Head Direction Cell Network

Calton, Jeffrey L.; Stackman, Robert W.; Goodridge, Jeremy P.; Archey, William B.; Dudchenko, Paul A.; Taube, Jeffrey S.

doi:10.1523/jneurosci.23-30-09719.2003

Cited by 164 publications

(171 citation statements)

References 52 publications

(51 reference statements)

Supporting

Mentioning

151

Contrasting

Unclassified

Order By: Relevance

“…Previous reports were ambiguous as to whether the AVN contained head direction cells (Taube, 1995;Calton et al, 2003), but one tetrode track in the present study clearly localized a head direction unit to the AVN (Fig. 2D).…”

Section: Head Direction Units In Multiple Thalamic Nucleicontrasting

confidence: 76%

Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells

Yoganarasimha¹,

Yu²,

Knierim³

2006

J. Neurosci.

133

149

View full text Add to dashboard Cite

Place cells of the hippocampal formation encode a spatial representation of the environment, and the orientation of this representation is apparently governed by the head direction cell system. The representation of a well explored environment by CA1 place cells can be split when there is conflicting information from salient proximal and distal cues, because some place fields rotate to follow the distal cues, whereas others rotate to follow the proximal cues (Knierim, 2002a). In contrast, the CA3 representation is more coherent than CA1, because the place fields in CA3 tend to rotate in the same direction (Lee et al., 2004). The present study tests whether the head direction cell network produces a split representation or remains coherent under these conditions by simultaneously recording both CA1 place cells and head direction cells from the thalamus. In agreement with previous studies, split representations of the environment were observed in ensembles of CA1 place cells in ϳ75% of the mismatch sessions, in which some fields followed the counterclockwise rotation of proximal cues and other fields followed the clockwise rotation of distal cues. However, of 225 recording sessions, there was not a single instance of the head direction cell ensembles revealing a split representation of head direction. Instead, in most of the mismatch sessions, the head direction cell tuning curves rotated as an ensemble clockwise (94%) and in a few sessions rotated counterclockwise (6%). The findings support the notion that the head direction cells may be part of an attractor network bound more strongly to distal landmarks than proximal landmarks, even under conditions in which the CA1 place representation loses its coherence.

show abstract

Section: Head Direction Units In Multiple Thalamic Nucleicontrasting

confidence: 76%

Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells

Yoganarasimha¹,

Yu²,

Knierim³

2006

J. Neurosci.

133

149

View full text Add to dashboard Cite

show abstract

“…It is thought that HC place cells and head direction cells found in CA1, postsubiculum, anterior dorsal thalamus, and lateral mammillary nuclei are interacting parts of the rodent navigational system (Leutgeb et al, 2000;Calton et al, 2003) that rely on allocentric and idiothetic information processing (Eichenbaum et al, 1990;Whishaw and Maaswinkel, 1998). Arc mRNA and protein localize in the dendrites against the activated synaptic inputs (Steward et al, 1998;Moga et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Gusev¹,

Cui²,

Alkon³

et al. 2005

J. Neurosci.

View full text Add to dashboard Cite

The understanding of the mechanisms of memory retrieval and its deficits, and the detection of memory underlying neuronal plasticity, is greatly impeded by a lack of precise knowledge of the brain circuitry that underlies the functions of memory. The specific roles of anatomically distinct hippocampal subdivisions in recent and long-term memory retention and recall are essentially unknown. To address these questions, we mapped the expression of Arc/Arg 3.1 mRNA, a neuronal activity marker, in memory retention at multiple rostrocaudal levels of the dentate gyrus, CA3, CA1, subiculum, and lateral and medial entorhinal cortices after a platform search in a water-maze spatial task at 24 h and 1 month compared with swim and naive controls. We found that the entorhinohippocampal neuronal activity underlying the recall of recent and remote spatial memory has an anatomically distributed and time-dependent organization throughout both the dorsal and ventral hippocampus that is subdivision specific. We found a dissociation in the activity of the entorhinal cortex, CA3, and CA1 over a period of memory consolidation. Although CA3, the dorsal hippocampus, and the entorhinal cortex demonstrated the most persistent learning-specific signal during both recent and long-term memory recall, CA1 and the ventral hippocampus displayed the most dramatic signal decline. We determined the coordinates of activity clusters in the hippocampal subdivisions during the platform search and their dynamics over time. Our mapping data suggest that although the level of corticohippocampal interaction is similar during the retrieval of recent and remote spatial memories, the mnemonic function of the hippocampus may have changed, and the activity underlying remote spatial memory could be anatomically segregated within hippocampal subdivisions in small segments.

show abstract

“…However, the activity of place cells is also influenced by other sensory and motor cues, including specific and nonspecific proximal cues, such as olfactory and somatosensory cues [4][5][6][7][8][9][10] , and locomotion cues such as optic flow and proprioception, which together with vestibular cues are thought to provide self-motion information for path integration [11][12][13] . Consistently, lesions of vestibular nuclei disrupt angular tuning of head-direction cells 14 and spatial tuning of hippocampal place cells 15 , although lesions of the headdirection cell network, which is thought to provide vestibular input to the hippocampus, do not substantially alter hippocampal spatial selectivity 16 . Additionally, the output of vestibular nuclei suppresses self-motion signals and depends on multisensory stimuli 17 .…”

mentioning

confidence: 84%

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

et al. 2014

View full text Add to dashboard Cite

During real-world (RW) exploration, rodent hippocampal activity shows robust spatial selectivity, which is hypothesized to be governed largely by distal visual cues, although other sensory-motor cues also contribute. Indeed, hippocampal spatial selectivity is weak in primate and human studies that use only visual cues. To determine the contribution of distal visual cues only, we measured hippocampal activity from body-fixed rodents exploring a two-dimensional virtual reality (VR). Compared to that in RW, spatial selectivity was markedly reduced during random foraging and goal-directed tasks in VR. Instead we found small but significant selectivity to distance traveled. Despite impaired spatial selectivity in VR, most spikes occurred within ~2-s-long hippocampal motifs in both RW and VR that had similar structure, including phase precession within motif fields. Selectivity to space and distance traveled were greatly enhanced in VR tasks with stereotypical trajectories. Thus, distal visual cues alone are insufficient to generate a robust hippocampal rate code for space but are sufficient for a temporal code. npg © 2015 Nature America, Inc. All rights reserved.1 2 2 VOLUME 18 | NUMBER 1 | JANUARY 2015 nature neurOSCIenCe a r t I C l e S same physical location in space can be approached from multiple different directions at different speeds. We thus investigated the contribution of distal visual cues only in determining selectivity in such an experimental setup. RESULTS Nature of spatial selectivity of hippocampal responsesWe measured hippocampal activity during a two-dimensional randomforaging task in RW and VR [35][36][37] with similar distal visual cues (Fig. 1a). In VR, the rats were body-fixed, i.e., their bodies were held in place, with a harness on a floating ball, allowing for head movements but precluding full-body turns, thus minimizing vestibular cues (Online Methods) 21,36 . Rats quickly learned to avoid the virtual edges entirely on the basis of visual cues 36 and spent a similar amount of time away from the edges and in the center of the platform (Fig. 1a) compared to in RW. We measured the activity of 1,066 and 1,238 principal neurons in RW and VR, respectively, in the dorsal CA1 of four rats under a variety of conditions (Online Methods). Neurons fired vigorously in restricted regions of space in RW, as expected (Fig. 1b,c, Supplementary Fig. 1a and Supplementary Video 1) 1 . In contrast, the neurons showed little spatial selectivity in VR during random foraging (Fig. 1b,d and Supplementary Fig. 1b).Across the ensemble, neurons had moderately reduced (25%) mean firing rates but greatly reduced (68%) peak firing rates in VR ( Fig. 2a and Supplementary Fig. 2a). Neurons in VR also had greatly reduced spatial information content (75%), stability (59%), sparsity (42%) and coherence (40%) (Fig. 2b-d and Supplementary Fig. 2b,c) compared to spatially localized, stable and sparse RW rate maps (Fig. 2c). Although the mean firing rate was inversely correlated with information content (Supplementary Fig. 2d)...

show abstract

Hippocampal Place Cell Instability after Lesions of the Head Direction Cell Network

Cited by 164 publications

References 52 publications

Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells

Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells

Topography of Arc/Arg3.1 mRNA Expression in the Dorsal and Ventral Hippocampus Induced by Recent and Remote Spatial Memory Recall: Dissociation of CA3 and CA1 Activation

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

Contact Info

Product

Resources

About