Proximodistal Segregation of Nonspatial Information in CA3: Preferential Recruitment of a Proximal CA3-Distal CA1 Network in Nonspatial Recognition Memory

Nakamura, N.; Flasbeck, Vera; Maingret, Nicolas; Kitsukawa, Takashi; Sauvage, Magdalena

doi:10.1523/jneurosci.4480-12.2013

Cited by 95 publications

(138 citation statements)

References 54 publications

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“…Of all cells with a place field at the odor port on the first day of training (which were observed in distal and proximal sectors), the spatial coding properties of proximal CA1 cells remained consistent throughout training, whereas distal CA1 cells gained odor modulation. Similarly, immediate early gene expression was reported in both proximal and distal CA1 in animals performing odor or object recognition tasks, but the expression was significantly higher in distal CA1 (Ito and Schuman, 2012;Nakamura et al, 2013). These findings are consistent with our observations that proximal CA1 appears primarily involved in the processing of spatial information, whereas other sectors can process nonspatial information.…”

Section: Discussionsupporting

confidence: 92%

“…To account for this potential confound, we performed the same analyses including data from only one session per animal (Well-Trained session). We found comparable mean effect sizes (see gray bars in Fig 3C-E Overall, these findings are consistent with other reports showing that nonspatial information processing is not evenly distributed along the proximodistal axis of CA1, including studies showing that odor or object information is more strongly represented in distal CA1 than in proximal CA1 (Ito and Schuman, 2012;Nakamura et al, 2013;Igarashi et al, 2014b). Our findings add to these studies by suggesting that functional dissociations may also extend to intermediate CA1, a region those previous reports did not specifically examine.…”

Section: Nonspatial Sequence Coding Was Not Uniformly Distributed Alosupporting

confidence: 92%

“…The present study extends these previous findings by providing the first characterization of the distribution of sequence coding (spatial or nonspatial), as well as a direct comparison with the distribution of place cell coding. Our study also complements previous work examining the distribution of nonspatial information, which has primarily focused on odor or object recognition memory (Ito and Schuman, 2012;Nakamura et al, 2013), by examining this coding in intermediate CA1 (in addition to distal and proximal CA1) in a paradigm that requires subjects to remember temporal relations among events, a critical contribution of the hippocampus to episodic memory (Fortin et al, 2002;Allen and Fortin, 2013;Howard and Eichenbaum, 2015).…”

Section: Discussionmentioning

confidence: 71%

“…Recent studies have indicated that the processing of spatial and nonspatial information is not uniformly distributed along the transverse (proximodistal) axis of CA1, with spatial information being preferentially represented in proximal CA1 (Henriksen et al, 2010;Oliva et al, 2016) and nonspatial information in distal CA1 (e.g., odors or objects; Burke et al, 2011;Ito and Schuman, 2012;Nakamura et al, 2013;Igarashi et al, 2014b). The main objective of the present study was to examine how sequence cells, which code for the temporal context in which events occurred (in this case, whether or not an odor was presented in the correct sequential order), were distributed along the same axis.…”

Section: Discussionmentioning

confidence: 99%

“…The two regions also show functional coupling during behavior, in the form of highly coherent oscillations in the 20-40 Hz range (Igarashi et al, 2014b). Similarly, expression of the immediate early gene Arc is higher in distal than proximal CA1 during nonspatial recognition memory performance (Nakamura et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Nonspatial sequence coding varies along the CA1 transverse axis

Elias

Asem

et al. 2018

Behavioural Brain Research

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The hippocampus plays a critical role in the memory for sequences of events, a defining feature of episodic memory. To shed light on the fundamental mechanisms supporting this capacity, we recently recorded neural activity in CA1 as rats performed a nonspatial odor sequence memory task. Our main finding was that, while the animals' location and behavior remained constant, a proportion of CA1 neurons fired differentially to odors depending on whether they were presented in or out of sequence (sequence cells). Here, we further examined if such sequence coding varied along the distal-to-proximal axis of the dorsal CA1 region (distal: toward subiculum; proximal: toward CA3). Differences in information processing along this axis have been suggested by recent anatomical and electrophysiological evidence that odor information may be more strongly represented in the distal segment, whereas spatial information may be more strongly represented in the proximal segment. Recorded neurons were grouped into four arbitrary sections of dorsal CA1, ranging from distal to proximal. We found that, although sequence cell coding was observed across the distal-to-proximal extent of CA1 from which we recorded, it was significantly higher in intermediate CA1, a region with more balanced anatomical input from lateral and medial entorhinal regions. More specifically, in that particular segment of CA1, we observed a significant increase in the magnitude of sequence coding of all cells, as well as in the sequential information content of sequence cells. Importantly, a different pattern was observed when examining the distribution of spatial coding from the same electrodes. Consistent with previous reports, our results suggest that spatial information was more strongly represented in the proximal section of CA1 (higher proportion of cells with place fields). These findings indicate that nonspatial sequence memory coding is not uniformly distributed along the transverse axis of CA1, and that this distribution does not simply follow the expected gradient based on the stimulus modality or the degree of spatial selectivity. Instead, the observed distribution suggests this form of sequence coding may be associated with convergent input from lateral and medial entorhinal regions, which is present throughout the proximodistal axis but higher in intermediate CA1.

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Section: Discussionsupporting

confidence: 92%

Section: Nonspatial Sequence Coding Was Not Uniformly Distributed Alosupporting

confidence: 92%

Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Nonspatial sequence coding varies along the CA1 transverse axis

Elias

Asem

et al. 2018

Behavioural Brain Research

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Spatial and stimulus-type tuning in the LEC, MEC, POR, PrC, CA1, and CA3 during spontaneous item recognition memory

et al. 2013

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According to the "two streams" hypothesis, the lateral entorhinal (LEC) and the perirhinal (PrC) cortices process information related to items (a "what" stream), the postrhinal (POR) and the medial entorhinal cortices (MEC) process spatial information (a "where" stream), and both types of information are integrated in the hippocampus (HIP). However, within the framework of memory function, only the HIP is reliably shown to preferentially process spatial information, and the PrC items' features. In contrast, the role of the LEC and MEC in memory is virtually unexplored, and conflicting results emerge for the POR. Moreover, the specific contribution of the hippocampal subfields CA1 and CA3 to spatial and non-spatial memory is not thoroughly understood. To investigate which of these areas is specifically tuned to spatial demands or stimulus identity (odor or object), we assessed the pattern of activation of these areas during recognition memory by detecting the immediate-early gene Arc, commonly used as a marker of neuronal activation. We report that all MTL areas were recruited during the spatial and the non-spatial tasks. However, the LEC, MEC, POR, and CA1 were activated to a comparable level in spatial and non-spatial tasks, while the PrC was tuned to stimulus-type, not spatial demands, and CA3 to spatial demands but not stimulus-type. Results are discussed within the frame of a recent model suggesting that the MTL could be segregated in terms of memory processes, such as recollection and familiarity, rather than information content.

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Intact CA3 in the hippocampus is only sufficient for contextual behavior based on well‐learned and unaltered visual background

Ahn

Lee

2014

Hippocampus

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Computational models suggest that the dentate gyrus and CA3 subfields of the hippocampus are responsible for discrete memory representations using pattern separation and pattern completion when a modified external stimulus is recognized as an old memory or encoded as a new memory. Experimental evidence of such computational processes in the hippocampus has been obtained mostly from spatial navigational tasks, and little is known about the proposed computational functions of the hippocampal subfields in "nonspatial" memory tasks. We tested whether rats with major damage in the dentate gyrus induced by colchicine lesions could remember patterned visual scene stimuli presented on LCD screens in the background. Rats responded using a touchscreen to indicate the identity of the visual scene. Performance of the lesion group was normal when tested with familiar visual scenes that had been learned prior to surgery. Lesioned rats exhibited severe deficits in learning novel visual scenes, but eventually reached the same level of performance as controls. However, unlike in controls, novel scene-associated memories formed in the lesion group were unstable and easily disrupted when ambiguous versions of the novel scenes were presented intermixed with the original stimuli. Our findings confirm that the prior computational models can also be applied to the nonspatial memory domain and suggest that the dentate gyrus is not necessary for the retrieval of learned visual scene-associated behavioral responses but plays a crucial role in forming novel visual scene-dependent memory and recognizing altered or ambiguous visual scenes in the background.

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Proximodistal Segregation of Nonspatial Information in CA3: Preferential Recruitment of a Proximal CA3-Distal CA1 Network in Nonspatial Recognition Memory

Cited by 95 publications

References 54 publications

Nonspatial sequence coding varies along the CA1 transverse axis

Nonspatial sequence coding varies along the CA1 transverse axis

Spatial and stimulus-type tuning in the LEC, MEC, POR, PrC, CA1, and CA3 during spontaneous item recognition memory

Intact CA3 in the hippocampus is only sufficient for contextual behavior based on well‐learned and unaltered visual background

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