Prefrontal Cortex Lesions Modify the Spatial Properties of Hippocampal Place Cells

Kyd, Rachel J.; Bilkey, David K.

doi:10.1093/cercor/13.5.444

Cited by 67 publications

(49 citation statements)

References 55 publications

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“…Accordingly, lesions of the mPFC do not prevent rats from being able to navigate through even quite complex spatial environments, like mazes (35). However, mPFC lesions do make hippocampal unit place fields less stable over time and more reactive to changes in the local environment (36,37). This result is consistent with the idea that the PFC might provide a more global representation of the spatial context (1,(38)(39)(40) that is independent of the subject's exact perspective.…”

supporting

confidence: 61%

Contextual encoding by ensembles of medial prefrontal cortex neurons

Hyman

Balaguer‐Ballester

et al. 2012

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

211

204

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Contextual representations serve to guide many aspects of behavior and influence the way stimuli or actions are encoded and interpreted. The medial prefrontal cortex (mPFC), including the anterior cingulate subregion, has been implicated in contextual encoding, yet the nature of contextual representations formed by the mPFC is unclear. Using multiple single-unit tetrode recordings in rats, we found that different activity patterns emerged in mPFC ensembles when animals moved between different environmental contexts. These differences in activity patterns were significantly larger than those observed for hippocampal ensembles. Whereas ≈11% of mPFC cells consistently preferred one environment over the other across multiple exposures to the same environments, optimal decoding (prediction) of the environmental setting occurred when the activity of up to ≈50% of all mPFC neurons was taken into account. On the other hand, population activity patterns were not identical upon repeated exposures to the very same environment. This was partly because the state of mPFC ensembles seemed to systematically shift with time, such that we could sometimes predict the change in ensemble state upon later reentry into one environment according to linear extrapolation from the time-dependent shifts observed during the first exposure. We also observed that many strongly action-selective mPFC neurons exhibited a significant degree of context-dependent modulation. These results highlight potential differences in contextual encoding schemes by the mPFC and hippocampus and suggest that the mPFC forms rich contextual representations that take into account not only sensory cues but also actions and time.electrophysiological recordings | population analysis | temporal encoding M any aspects of behavior are contextually dependent. Contexts can be abstract, as in the case of human language, or can be more concrete and be defined by the constellation of spatial and sensory stimuli surrounding an individual. Contextual representations can form quickly and tend to remain stable despite local variations in perspective (1). Context can also help to inform the subject about potential changes in the meaning of stimuli and actions. The medial prefrontal cortex (mPFC) is involved in various forms of cognition that depend on spatial and contextual information, including context-based cognitive tasks (2-4), contextual fear conditioning (5), and context-induced drug relapse (6-8), and is believed to be an important node in the "context" network (1, 9-12). These functions likely depend on reciprocal interactions with the hippocampus (13, 14), an area that has a well-established role in spatial and contextual processing (15)(16)(17)(18)(19)(20). Through the connection from the CA1 region, the hippocampus has multiple profound effects on mPFC neurons (21-28), and it has been proposed that during spatial navigation the mPFC may work in concert with the hippocampus to encode goal locations and aid in route planning (29,30). However, the spatial representations ...

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supporting

confidence: 61%

Contextual encoding by ensembles of medial prefrontal cortex neurons

Hyman

Balaguer‐Ballester

et al. 2012

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

211

204

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“…In this circuit, mPFC receiving convergent input from multiple brain regions (Conde et al, 1995) would help EC to develop a spatial map with its integrated information. This hypothesis is supported by observations that mPFC neurons are capable of monitoring spatial information (Hok et al, 2005) and that mPFC lesions alter hippocampal place cell activity after a long-term delay (Kyd and Bilkey, 2003). Thus, in the full-cue environment, the visual cortex may provide EC with robust allocentric input, sufficient to recall the whole spatial memory regardless of mPFC (Nakazawa et al, 2002).…”

Section: Ca3 and Spatial Memory Acquisitionmentioning

confidence: 78%

The Medial Prefrontal Cortex Is Involved in Spatial Memory Retrieval under Partial-Cue Conditions

Jo¹,

Park²,

Kim³

et al. 2007

J. Neurosci.

113

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Brain circuits involved in pattern completion, or retrieval of memory from fragmented cues, were investigated. Using different versions of the Morris water maze, we explored the roles of the CA3 subregion of the hippocampus and the medial prefrontal cortex (mPFC) in spatial memory retrieval under various conditions. In a hidden platform task, both CA3 and mPFC lesions disrupted memory retrieval under partial-cue, but not under full-cue, conditions. For a delayed matching-to-place task, CA3 lesions produced a deficit in both forming and recalling spatial working memory regardless of extramaze cue conditions. In contrast, damage to mPFC impaired memory retrieval only when a fraction of cues was available. To corroborate the lesion study, we examined the expression of the immediate early gene c-fos in mPFC and the hippocampus. After training of spatial reference memory in full-cue conditions for 6 d, the same training procedure in the absence of all cues except one increased the number of Fos-immunoreactive cells in mPFC and CA3. Furthermore, mPFC inactivation with muscimol, a GABA agonist, blocked memory retrieval in the degraded-cue environment. However, mPFC-lesioned animals initially trained in a single-cue environment had no difficulty in retrieving spatial memory when the number of cues was increased, demonstrating that contextual change per se did not impair the behavioral performance of the mPFC-lesioned animals. Together, these findings strongly suggest that pattern completion requires interactions between mPFC and the hippocampus, in which mPFC plays significant roles in retrieving spatial information maintained in the hippocampus for efficient navigation.

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“…The observation that hippocampal place cell activity is altered after large mPFC lesions clearly suggests dynamic interactions between these two brain structures (43). Further assessment of these interactions will therefore require simultaneous recordings of mPFC cells and hippocampal place cells.…”

Section: Discussionmentioning

confidence: 99%

Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex

Hok

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Lenck-Santini

et al. 2005

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

231

181

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Finding one's way in space requires a distributed neural network to support accurate spatial navigation. In the rat, this network likely includes the hippocampus and its place cells. Although such cells allow the organism to locate itself in the environment, an additional mechanism is required to specify the animal's goal. Here, we show that firing activity of neurons in medial prefrontal cortex (mPFC) reflects the motivational salience of places. We recorded mPFC neurons from rats performing a place navigation task, and found that a substantial proportion of cells in the prelimbic͞infralimbic area had place fields. A much smaller proportion of cells with such properties was found in the dorsal anterior cingulate area. Furthermore, the distribution of place fields in prelimbic͞infralimbic cells was not homogeneous: goal locations were overrepresented. Because such locations were spatially dissociated from rewards, we suggest that mPFC neurons might be responsible for encoding the rat's goals, a process necessary for path planning.goal coding ͉ place navigation ͉ unit recording

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Prefrontal Cortex Lesions Modify the Spatial Properties of Hippocampal Place Cells

Cited by 67 publications

References 55 publications

Contextual encoding by ensembles of medial prefrontal cortex neurons

Contextual encoding by ensembles of medial prefrontal cortex neurons

The Medial Prefrontal Cortex Is Involved in Spatial Memory Retrieval under Partial-Cue Conditions

Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex

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