Objects and landmarks: Hippocampal place cells respond differently to manipulations of visual cues depending on size, perspective, and experience

Scaplen, Kristin M.; Gulati, Arune A.; Heimer-McGinn, Victoria; Burwell, Rebecca D.

doi:10.1002/hipo.22331

Cited by 30 publications

(32 citation statements)

References 48 publications

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“…Moreover, our model is also in line with the elevated sensitivity of the neuronal responses to any change in the environment (e.g. the delivery of reward (12,58), or the manipulation of landmarks (59,60)). This phenomenon is often described as "remapping" (61) and is widely observed in experiments.…”

Section: Discussionsupporting

confidence: 71%

Are place cells just memory cells? Memory compression leads to spatial tuning and history dependence

Fusi

2019

Preprint

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The observation of place cells has suggested that the hippocampus plays a special role in encoding spatial information. However, place cell responses are modulated by several non-spatial variables, and reported to be rather unstable. Here we propose a memory model of the hippocampus that provides a novel interpretation of place cells consistent with these observations. We hypothesize that the hippocampus is a memory device that takes advantage of the correlations between sensory experiences to generate compressed representations of the episodes that are stored in memory. A simple neural network model that can efficiently compress information naturally produces place cells that are similar to those observed in experiments. It predicts that the activity of these cells is variable and that the fluctuations of the place fields encode information about the recent history of sensory experiences. Place cells may simply be a consequence of a memory compression process implemented in the hippocampus.

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Section: Discussionsupporting

confidence: 71%

Are place cells just memory cells? Memory compression leads to spatial tuning and history dependence

Fusi

2019

Preprint

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“…The PER provides this information to the hippocampus for associative learning, for example, when a particular object is rewarded in one context but not another. Indeed, a number of studies have reported that the hippocampus responds to objects as well as places, contexts, and landmarks (Komorowski et al, 2009;Deshmukh and Knierim, 2013;Scaplen et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Disconnection of the Perirhinal and Postrhinal Cortices Impairs Recognition of Objects in Context But Not Contextual Fear Conditioning

et al. 2017

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The perirhinal cortex (PER) is known to process object information, whereas the rodent postrhinal cortex (POR), homolog to the parahippocampal cortex in primates, is thought to process spatial information. A number of studies, however, provide evidence that both areas are involved in processing contextual information. In this study, we tested the hypothesis that the rat POR relies on object information received from the PER to form complex representations of context. Using three fear-conditioning (FC) paradigms (signaled, unsignaled, and renewal) and two context-guided object recognition tasks (with 3D and 2D objects), we examined the effects of crossed excitotoxic lesions to the POR and the contralateral PER. Performance of rats with crossed lesions was compared with that of rats with ipsilateral POR plus PER lesions and sham-operated rats. We found that rats with contralateral PER-POR lesions were impaired in object-context recognition but not in contextual FC. Therefore, interaction between the POR and PER is necessary for context-guided exploratory behavior but not for associating fear with context. Our results provide evidence for the hypothesis that the POR relies on object and pattern information from the PER to encode representations of context. The association of fear with a context, however, may be supported by alternate cortical and/or subcortical pathways when PER-POR interaction is not available. Our results suggest that contextual FC may represent a special case of context-guided behavior. Representations of context are important for perception, memory, decision making, and other cognitive processes. Moreover, there is extensive evidence that the use of contextual representations to guide appropriate behavior is disrupted in neuropsychiatric and neurological disorders including developmental disorders, schizophrenia, affective disorders, and Alzheimer's disease. Many of these disorders are accompanied by changes in parahippocampal and hippocampal structures. Understanding how context is represented in the brain and how parahippocampal structures are involved will enhance our understanding and treatment of the cognitive and behavioral symptoms associated with neurological disorders and neuropsychiatric disease.

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“…Place field responses within a condition were classified as rotation, remap or no change as previously described (Scaplen et al, 2014). Briefly, place fields were classified as having predictably rotated if the field rotated at least once in concert with the rotation of the relevant cue.…”

Section: Methodsmentioning

confidence: 99%

Inactivation of the Lateral Entorhinal Area Increases the Influence of Visual Cues on Hippocampal Place Cell Activity

Scaplen

Ramesh

Nadvar

et al. 2017

Front. Syst. Neurosci.

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The hippocampus is important for both navigation and associative learning. We previously showed that the hippocampus processes two-dimensional (2D) landmarks and objects differently. Our findings suggested that landmarks are more likely to be used for orientation and navigation, whereas objects are more likely to be used for associative learning. The process by which cues are recognized as relevant for navigation or associative learning, however, is an open question. Presumably both spatial and nonspatial information are necessary for classifying cues as landmarks or objects. The lateral entorhinal area (LEA) is a good candidate for participating in this process as it is implicated in the processing of three-dimensional (3D) objects and object location. Because the LEA is one synapse upstream of the hippocampus and processes both spatial and nonspatial information, it is reasonable to hypothesize that the LEA modulates how the hippocampus uses 2D landmarks and objects. To test this hypothesis, we temporarily inactivated the LEA ipsilateral to the dorsal hippocampal recording site using fluorophore-conjugated muscimol (FCM) 30 min prior to three foraging sessions in which either the 2D landmark or the 2D object was back-projected to the floor of an open field. Prior to the second session we rotated the 2D cue by 90°. Cues were returned to the original configuration for the third session. Compared to the Saline treatment, FCM inactivation increased the percentage of rotation responses to manipulations of the landmark cue, but had no effect on information content of place fields. In contrast, FCM inactivation increased information content of place fields in the presence of the object cue, but had no effect on rotation responses to the object cue. Thus, LEA inactivation increased the influence of visual cues on hippocampal activity, but the impact was qualitatively different for cues that are useful for navigation vs. cues that may not be useful for navigation. FCM inactivation also led to reductions in both frequency and power of hippocampal theta rhythms, indicative of the loss of functionally important LEA inputs to hippocampus. These data provide evidence that the LEA is involved in modulating how the dorsal hippocampus utilizes visual environmental cues.

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Objects and landmarks: Hippocampal place cells respond differently to manipulations of visual cues depending on size, perspective, and experience

Cited by 30 publications

References 48 publications

Are place cells just memory cells? Memory compression leads to spatial tuning and history dependence

Are place cells just memory cells? Memory compression leads to spatial tuning and history dependence

Disconnection of the Perirhinal and Postrhinal Cortices Impairs Recognition of Objects in Context But Not Contextual Fear Conditioning

Inactivation of the Lateral Entorhinal Area Increases the Influence of Visual Cues on Hippocampal Place Cell Activity

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