HippocampusPub Date : 2024-05-09DOI: 10.1002/hipo.23607
Matthew Buckley, Anthony McGregor, Niklas Ihssen, Joseph Austen, Simon Thurlbeck, Shamus P. Smith, Armin Heinecke, Adina R. Lew
{"title":"The well-worn route revisited: Striatal and hippocampal system contributions to familiar route navigation","authors":"Matthew Buckley, Anthony McGregor, Niklas Ihssen, Joseph Austen, Simon Thurlbeck, Shamus P. Smith, Armin Heinecke, Adina R. Lew","doi":"10.1002/hipo.23607","DOIUrl":"10.1002/hipo.23607","url":null,"abstract":"<p>Classic research has shown a division in the neuroanatomical structures that support flexible (e.g., short-cutting) and habitual (e.g., familiar route following) navigational behavior, with hippocampal–caudate systems associated with the former and putamen systems with the latter. There is, however, disagreement about whether the neural structures involved in navigation process particular forms of spatial information, such as associations between constellations of cues forming a cognitive map, versus single landmark-action associations, or alternatively, perform particular reinforcement learning algorithms that allow the use of different spatial strategies, so-called model-based (flexible) or model-free (habitual) forms of learning. We sought to test these theories by asking participants (<i>N</i> = 24) to navigate within a virtual environment through a previously learned, 9-junction route with distinctive landmarks at each junction while undergoing functional magnetic resonance imaging (fMRI). In a series of probe trials, we distinguished knowledge of individual landmark-action associations along the route versus knowledge of the correct <i>sequence</i> of landmark-action associations, either by having absent landmarks, or “out-of-sequence” landmarks. Under a map-based perspective, sequence knowledge would not require hippocampal systems, because there are no constellations of cues available for cognitive map formation. Within a learning-based model, however, responding based on knowledge of sequence <i>would</i> require hippocampal systems because prior context has to be utilized. We found that hippocampal–caudate systems were more active in probes requiring sequence knowledge, supporting the learning-based model. However, we also found greater putamen activation in probes where navigation based purely on sequence memory could be planned, supporting models of putamen function that emphasize its role in action sequencing.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 7","pages":"310-326"},"PeriodicalIF":2.4,"publicationDate":"2024-05-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23607","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140891024","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
HippocampusPub Date : 2024-05-03DOI: 10.1002/hipo.23608
Blake L. Elliott, Raana A. Mohyee, Ian C. Ballard, Ingrid R. Olson, Lauren M. Ellman, Vishnu P. Murty
{"title":"In vivo structural connectivity of the reward system along the hippocampal long axis","authors":"Blake L. Elliott, Raana A. Mohyee, Ian C. Ballard, Ingrid R. Olson, Lauren M. Ellman, Vishnu P. Murty","doi":"10.1002/hipo.23608","DOIUrl":"10.1002/hipo.23608","url":null,"abstract":"<p>Recent work has identified a critical role for the hippocampus in reward-sensitive behaviors, including motivated memory, reinforcement learning, and decision-making. Animal histology and human functional neuroimaging have shown that brain regions involved in reward processing and motivation are more interconnected with the ventral/anterior hippocampus. However, direct evidence examining gradients of structural connectivity between reward regions and the hippocampus in humans is lacking. The present study used diffusion MRI (dMRI) and probabilistic tractography to quantify the structural connectivity of the hippocampus with key reward processing regions in vivo. Using a large sample of subjects (<i>N</i> = 628) from the human connectome dMRI data release, we found that connectivity profiles with the hippocampus varied widely between different regions of the reward circuit. While the dopaminergic midbrain (ventral tegmental area) showed stronger connectivity with the anterior versus posterior hippocampus, the ventromedial prefrontal cortex showed stronger connectivity with the posterior hippocampus. The limbic (ventral) striatum demonstrated a more homogeneous connectivity profile along the hippocampal long axis. This is the first study to generate a probabilistic atlas of the hippocampal structural connectivity with reward-related networks, which is essential to investigating how these circuits contribute to normative adaptive behavior and maladaptive behaviors in psychiatric illness. These findings describe nuanced structural connectivity that sets the foundation to better understand how the hippocampus influences reward-guided behavior in humans.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 7","pages":"327-341"},"PeriodicalIF":2.4,"publicationDate":"2024-05-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140835429","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
HippocampusPub Date : 2024-04-09DOI: 10.1002/hipo.23606
Alice L. Hickling, Ian A. Clark, Yan I. Wu, Eleanor A. Maguire
{"title":"Automated protocols for delineating human hippocampal subfields from 3 Tesla and 7 Tesla magnetic resonance imaging data","authors":"Alice L. Hickling, Ian A. Clark, Yan I. Wu, Eleanor A. Maguire","doi":"10.1002/hipo.23606","DOIUrl":"10.1002/hipo.23606","url":null,"abstract":"<p>Researchers who study the human hippocampus are naturally interested in how its subfields function. However, many researchers are precluded from examining subfields because their manual delineation from magnetic resonance imaging (MRI) scans (still the gold standard approach) is time consuming and requires significant expertise. To help ameliorate this issue, we present here two protocols, one for 3T MRI and the other for 7T MRI, that permit automated hippocampus segmentation into six subregions, namely dentate gyrus/cornu ammonis (CA)4, CA2/3, CA1, subiculum, pre/parasubiculum, and uncus along the entire length of the hippocampus. These protocols are particularly notable relative to existing resources in that they were trained and tested using large numbers of healthy young adults (n = 140 at 3T, n = 40 at 7T) whose hippocampi were manually segmented by experts from MRI scans. Using inter-rater reliability analyses, we showed that the quality of automated segmentations produced by these protocols was high and comparable to expert manual segmenters. We provide full open access to the automated protocols, and anticipate they will save hippocampus researchers a significant amount of time. They could also help to catalyze subfield research, which is essential for gaining a full understanding of how the hippocampus functions.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 6","pages":"302-308"},"PeriodicalIF":3.5,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23606","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140584527","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
HippocampusPub Date : 2024-03-23DOI: 10.1002/hipo.23605
Akul Satish, Vanessa G. Keller, Sumaiyah Raza, Shona Fitzpatrick, Aidan J. Horner
{"title":"Theta and alpha oscillations in human hippocampus and medial parietal cortex support the formation of location-based representations","authors":"Akul Satish, Vanessa G. Keller, Sumaiyah Raza, Shona Fitzpatrick, Aidan J. Horner","doi":"10.1002/hipo.23605","DOIUrl":"10.1002/hipo.23605","url":null,"abstract":"<p>Our ability to navigate in a new environment depends on learning new locations. Mental representations of locations are quickly accessible during navigation and allow us to know where we are regardless of our current viewpoint. Recent functional magnetic resonance imaging (fMRI) research using pattern classification has shown that these location-based representations emerge in the retrosplenial cortex and parahippocampal gyrus, regions theorized to be critically involved in spatial navigation. However, little is currently known about the oscillatory dynamics that support the formation of location-based representations. We used magnetoencephalogram (MEG) recordings to investigate region-specific oscillatory activity in a task where participants could form location-based representations. Participants viewed videos showing that two perceptually distinct scenes (180° apart) belonged to the same location. This “overlap” video allowed participants to bind the two distinct scenes together into a more coherent location-based representation. Participants also viewed control “non-overlap” videos where two distinct scenes from two different locations were shown, where no location-based representation could be formed. In a post-video behavioral task, participants successfully matched the two viewpoints shown in the overlap videos, but not the non-overlap videos, indicating they successfully learned the locations in the overlap condition. Comparing oscillatory activity between the overlap and non-overlap videos, we found greater theta and alpha/beta power during the overlap relative to non-overlap videos, specifically at time-points when we expected scene integration to occur. These oscillations localized to regions in the medial parietal cortex (precuneus and retrosplenial cortex) and the medial temporal lobe, including the hippocampus. Therefore, we find that theta and alpha/beta oscillations in the hippocampus and medial parietal cortex are likely involved in the formation of location-based representations.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 6","pages":"284-301"},"PeriodicalIF":3.5,"publicationDate":"2024-03-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23605","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140193638","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
HippocampusPub Date : 2024-03-22DOI: 10.1002/hipo.23603
Patrick A. Forcelli, Elyssa M. LaFlamme, Hannah F. Waguespack, Richard C. Saunders, Ludise Malkova
{"title":"Hippocampal lesions impair non-navigational spatial memory in macaques","authors":"Patrick A. Forcelli, Elyssa M. LaFlamme, Hannah F. Waguespack, Richard C. Saunders, Ludise Malkova","doi":"10.1002/hipo.23603","DOIUrl":"10.1002/hipo.23603","url":null,"abstract":"<p>Decades of studies robustly support a critical role for the hippocampus in spatial memory across a wide range of species. Hippocampal damage produces clear and consistent deficits in allocentric spatial memory that requires navigating through space in rodents, non-human primates, and humans. By contrast, damage to the hippocampus spares performance in most non-navigational spatial memory tasks—which can typically be resolved using egocentric cues. We previously found that transient inactivation of the hippocampus impairs performance in the Hamilton Search Task (HST), a self-ordered non-navigational spatial search task. A key question, however, still needs to be addressed. Acute, reversible inactivation of the hippocampus may have resulted in an impairment in the HST because this approach does not allow for neuroplastic compensation, may prevent the development of an alternative learning strategy, and/or may produce network-based effects that disrupt performance. We compared learning and performance on the HST in male rhesus macaques (six unoperated control animals and six animals that underwent excitotoxic lesions of the hippocampus). We found a significant impairment in animals with hippocampal lesions. While control animals improved in performance over the course of 45 days of training, performance in animals with hippocampal lesions remained at chance levels. The HST thus represents a sensitive assay for probing the integrity of the hippocampus in non-human primates. These data provide evidence demonstrating that the hippocampus is critical for this type of non-navigational spatial memory, and help to reconcile the many null findings previously reported.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 5","pages":"261-275"},"PeriodicalIF":3.5,"publicationDate":"2024-03-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140184267","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
HippocampusPub Date : 2024-03-19DOI: 10.1002/hipo.23604
Krista A. Mitchnick, Hannah Marlatte, Zorry Belchev, Fuqiang Gao, R. Shayna Rosenbaum
{"title":"Differential contributions of the hippocampal dentate gyrus and CA1 subfield to mnemonic discrimination","authors":"Krista A. Mitchnick, Hannah Marlatte, Zorry Belchev, Fuqiang Gao, R. Shayna Rosenbaum","doi":"10.1002/hipo.23604","DOIUrl":"10.1002/hipo.23604","url":null,"abstract":"<p>Evidence suggests that individual hippocampal subfields are preferentially involved in various memory-related processes. Here, we demonstrated dissociations in these memory processes in two unique individuals with near-selective bilateral damage within the hippocampus, affecting the dentate gyrus (DG) in case BL and the cornu ammonis 1 (CA1) subfield in case BR. BL was impaired in discriminating highly similar objects in memory (i.e., mnemonic discrimination) but exhibited preserved overall recognition of studied objects, regardless of similarity. Conversely, BR demonstrated impaired general recognition. These results provide evidence for the DG in discrimination processes, likely related to underlying pattern separation computations, and the CA1 in retention/retrieval.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 6","pages":"278-283"},"PeriodicalIF":3.5,"publicationDate":"2024-03-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23604","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140158050","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
HippocampusPub Date : 2024-02-28DOI: 10.1002/hipo.23602
Anika Wuestefeld, Hannah Baumeister, Jenna N. Adams, Robin de Flores, Carl J. Hodgetts, Negar Mazloum-Farzaghi, Rosanna K. Olsen, Vyash Puliyadi, Tammy T. Tran, Arnold Bakker, Kelsey L. Canada, Marshall A. Dalton, Ana M. Daugherty, Renaud La Joie, Lei Wang, Madigan L. Bedard, Esther Buendia, Eunice Chung, Amanda Denning, María del Mar Arroyo-Jiménez, Emilio Artacho-Pérula, David J. Irwin, Ranjit Ittyerah, Edward B. Lee, Sydney Lim, María del Pilar Marcos-Rabal, Maria Mercedes Iñiguez de Onzoño Martin, Monica Munoz Lopez, Carlos de la Rosa Prieto, Theresa Schuck, Winifred Trotman, Alicia Vela, Paul Yushkevich, Katrin Amunts, Jean C. Augustinack, Song-Lin Ding, Ricardo Insausti, Olga Kedo, David Berron, Laura E. M. Wisse
{"title":"Comparison of histological delineations of medial temporal lobe cortices by four independent neuroanatomy laboratories","authors":"Anika Wuestefeld, Hannah Baumeister, Jenna N. Adams, Robin de Flores, Carl J. Hodgetts, Negar Mazloum-Farzaghi, Rosanna K. Olsen, Vyash Puliyadi, Tammy T. Tran, Arnold Bakker, Kelsey L. Canada, Marshall A. Dalton, Ana M. Daugherty, Renaud La Joie, Lei Wang, Madigan L. Bedard, Esther Buendia, Eunice Chung, Amanda Denning, María del Mar Arroyo-Jiménez, Emilio Artacho-Pérula, David J. Irwin, Ranjit Ittyerah, Edward B. Lee, Sydney Lim, María del Pilar Marcos-Rabal, Maria Mercedes Iñiguez de Onzoño Martin, Monica Munoz Lopez, Carlos de la Rosa Prieto, Theresa Schuck, Winifred Trotman, Alicia Vela, Paul Yushkevich, Katrin Amunts, Jean C. Augustinack, Song-Lin Ding, Ricardo Insausti, Olga Kedo, David Berron, Laura E. M. Wisse","doi":"10.1002/hipo.23602","DOIUrl":"10.1002/hipo.23602","url":null,"abstract":"<p>The medial temporal lobe (MTL) cortex, located adjacent to the hippocampus, is crucial for memory and prone to the accumulation of certain neuropathologies such as Alzheimer's disease neurofibrillary tau tangles. The MTL cortex is composed of several subregions which differ in their functional and cytoarchitectonic features. As neuroanatomical schools rely on different cytoarchitectonic definitions of these subregions, it is unclear to what extent their delineations of MTL cortex subregions overlap. Here, we provide an overview of cytoarchitectonic definitions of the entorhinal and parahippocampal cortices as well as Brodmann areas (BA) 35 and 36, as provided by four neuroanatomists from different laboratories, aiming to identify the rationale for overlapping and diverging delineations. Nissl-stained series were acquired from the temporal lobes of three human specimens (two right and one left hemisphere). Slices (50 μm thick) were prepared perpendicular to the long axis of the hippocampus spanning the entire longitudinal extent of the MTL cortex. Four neuroanatomists annotated MTL cortex subregions on digitized slices spaced 5 mm apart (pixel size 0.4 μm at 20× magnification). Parcellations, terminology, and border placement were compared among neuroanatomists. Cytoarchitectonic features of each subregion are described in detail. Qualitative analysis of the annotations showed higher agreement in the definitions of the entorhinal cortex and BA35, while the definitions of BA36 and the parahippocampal cortex exhibited less overlap among neuroanatomists. The degree of overlap of cytoarchitectonic definitions was partially reflected in the neuroanatomists' agreement on the respective delineations. Lower agreement in annotations was observed in transitional zones between structures where seminal cytoarchitectonic features are expressed less saliently. The results highlight that definitions and parcellations of the MTL cortex differ among neuroanatomical schools and thereby increase understanding of why these differences may arise. This work sets a crucial foundation to further advance anatomically-informed neuroimaging research on the human MTL cortex.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 5","pages":"241-260"},"PeriodicalIF":3.5,"publicationDate":"2024-02-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23602","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139982822","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}