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}
HippocampusPub Date : 2024-02-23DOI: 10.1002/hipo.23601
Jordana Griebler Luft, Bruno Popik, Débora Aguirre Gonçalves, Fabio Cardoso Cruz, Lucas de Oliveira Alvares
{"title":"Distinct engrams control fear and extinction memory","authors":"Jordana Griebler Luft, Bruno Popik, Débora Aguirre Gonçalves, Fabio Cardoso Cruz, Lucas de Oliveira Alvares","doi":"10.1002/hipo.23601","DOIUrl":"10.1002/hipo.23601","url":null,"abstract":"<p>Memories are stored in engram cells, which are necessary and sufficient for memory recall. Recalling a memory might undergo reconsolidation or extinction. It has been suggested that the original memory engram is reactivated during reconsolidation so that memory can be updated. Conversely, during extinction training, a new memory is formed that suppresses the original engram. Nonetheless, it is unknown whether extinction creates a new engram or modifies the original fear engram. In this study, we utilized the Daun02 procedure, which uses c-Fos-lacZ rats to induce apoptosis of strongly activated neurons and examine whether a new memory trace emerges as a result of a short or long reactivation, or if these processes rely on modifications within the original engram located in the basolateral amygdala (BLA) and infralimbic (IL) cortex. By eliminating neurons activated during consolidation and reactivation, we observed significant impacts on fear memory, highlighting the importance of the BLA engram in these processes. Although we were unable to show any impact when removing the neurons activated after the test of a previously extinguished memory in the BLA, disrupting the IL extinction engram reactivated the aversive memory that was suppressed by the extinction memory. Thus, we demonstrated that the IL cortex plays a crucial role in the network involved in extinction, and disrupting this specific node alone is sufficient to impair extinction behavior. Additionally, our findings indicate that extinction memories rely on the formation of a new memory, supporting the theory that extinction memories rely on the formation of a new memory, whereas the reconsolidation process reactivates the same original memory trace.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 5","pages":"230-240"},"PeriodicalIF":3.5,"publicationDate":"2024-02-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139939949","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 : 2024-02-16DOI: 10.1002/hipo.23600
Svitlana V. Bach, Allison J. Bauman, Darya Hosein, Jennifer J. Tuscher, Lara Ianov, Kelsey M. Greathouse, Benjamin W. Henderson, Jeremy H. Herskowitz, Keri Martinowich, Jeremy J. Day
{"title":"Distinct roles of Bdnf I and Bdnf IV transcript variant expression in hippocampal neurons","authors":"Svitlana V. Bach, Allison J. Bauman, Darya Hosein, Jennifer J. Tuscher, Lara Ianov, Kelsey M. Greathouse, Benjamin W. Henderson, Jeremy H. Herskowitz, Keri Martinowich, Jeremy J. Day","doi":"10.1002/hipo.23600","DOIUrl":"10.1002/hipo.23600","url":null,"abstract":"<p>Brain-derived neurotrophic factor (<i>Bdnf</i>) plays a critical role in brain development, dendritic growth, synaptic plasticity, as well as learning and memory. The rodent <i>Bdnf</i> gene contains nine 5′ non-coding exons (<i>I</i>–<i>IXa</i>), which are spliced to a common 3′ coding exon (<i>IX</i>). Transcription of individual <i>Bdnf</i> variants, which all encode the same BDNF protein, is initiated at unique promoters upstream of each non-coding exon, enabling precise spatiotemporal and activity-dependent regulation of <i>Bdnf</i> expression. Although prior evidence suggests that <i>Bdnf</i> transcripts containing exon <i>I</i> (<i>Bdnf I</i>) or exon <i>IV</i> (<i>Bdnf IV</i>) are uniquely regulated by neuronal activity, the functional significance of different <i>Bdnf</i> transcript variants remains unclear. To investigate functional roles of activity-dependent <i>Bdnf I</i> and <i>IV</i> transcripts, we used a CRISPR activation system in which catalytically dead Cas9 fused to a transcriptional activator (VPR) is targeted to individual <i>Bdnf</i> promoters with single guide RNAs, resulting in transcript-specific <i>Bdnf</i> upregulation. <i>Bdnf I</i> upregulation is associated with gene expression changes linked to dendritic growth, while <i>Bdnf IV</i> upregulation is associated with genes that regulate protein catabolism. Upregulation of <i>Bdnf I</i>, but not <i>Bdnf IV</i>, increased mushroom spine density, volume, length, and head diameter, and also produced more complex dendritic arbors in cultured rat hippocampal neurons. In contrast, upregulation of <i>Bdnf IV</i>, but not <i>Bdnf I</i>, in the rat hippocampus attenuated contextual fear expression. Our data suggest that while <i>Bdnf I</i> and <i>IV</i> are both activity-dependent, BDNF produced from these promoters may serve unique cellular, synaptic, and behavioral functions.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 5","pages":"218-229"},"PeriodicalIF":3.5,"publicationDate":"2024-02-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23600","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139740940","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 : 2024-01-12DOI: 10.1002/hipo.23599
Agustina Fragueiro, Claire Cury, Federica Santacroce, Ford Burles, Giuseppe Iaria, Giorgia Committeri
{"title":"Medial positioning of the hippocampus and hippocampal fissure volume in developmental topographical disorientation","authors":"Agustina Fragueiro, Claire Cury, Federica Santacroce, Ford Burles, Giuseppe Iaria, Giorgia Committeri","doi":"10.1002/hipo.23599","DOIUrl":"10.1002/hipo.23599","url":null,"abstract":"<p>Developmental topographical disorientation (DTD) refers to the lifelong inability to orient by means of cognitive maps in familiar surroundings despite otherwise well-preserved general cognitive functions, and the absence of any acquired brain injury or neurological condition. While reduced functional connectivity between the hippocampus and other brain regions has been reported in DTD individuals, no structural differences in gray matter tissue for the whole brain neither for the hippocampus were detected. Considering that the human hippocampus is the main structure associated with cognitive map-based navigation, here, we investigated differences in morphological and morphometric hippocampal features between individuals affected by DTD (<i>N</i> = 20) and healthy controls (<i>N</i> = 238). Specifically, we focused on a developmental anomaly of the hippocampus that is characterized by the incomplete infolding of hippocampal subfields during fetal development, giving the hippocampus a more round or pyramidal shape, called incomplete hippocampal inversion (IHI). We rated IHI according to standard criteria and extracted hippocampal subfield volumes after FreeSurfer's automatic segmentation. We observed similar IHI prevalence in the group of individuals with DTD with respect to the control population. Neither differences in whole hippocampal nor major hippocampal subfield volumes have been observed between groups. However, when assessing the IHI independent criteria, we observed that the hippocampus in the DTD group is more medially positioned comparing to the control group. In addition, we observed bigger hippocampal fissure volume for the DTD comparing to the control group. Both of these findings were stronger for the right hippocampus comparing to the left. Our results provide new insights regarding the hippocampal morphology of individuals affected by DTD, highlighting the role of structural anomalies during early prenatal development in line with the developmental nature of the spatial disorientation deficit.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 4","pages":"204-216"},"PeriodicalIF":3.5,"publicationDate":"2024-01-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139424671","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 : 2024-01-08DOI: 10.1002/hipo.23597
David G. Amaral, Jean Augustinack, Helen Barbas, Matthew Frosch, John Gabrieli, Jennifer Luebke, Pasko Rakic, Douglas Rosene, Richard J. Rushmore
{"title":"The analysis of H.M.'s brain: A brief review of status and plans for future studies and tissue archive","authors":"David G. Amaral, Jean Augustinack, Helen Barbas, Matthew Frosch, John Gabrieli, Jennifer Luebke, Pasko Rakic, Douglas Rosene, Richard J. Rushmore","doi":"10.1002/hipo.23597","DOIUrl":"10.1002/hipo.23597","url":null,"abstract":"<p>The famous amnesic patient Henry Molaison (H.M.) died on December 2, 2008. After extensive in situ magnetic resonance imaging in Boston, his brain was removed at autopsy and transported to the University of California San Diego. There the brain was prepared for frozen sectioning and cut into 2401, 70 μm coronal slices. While preliminary analyses of the brain sections have been reported, a comprehensive microscopic neuroanatomical analysis of the state of H.M.'s brain at the time of his death has not yet been published. The brain tissue and slides were subsequently moved to the University of California Davis and the slides digitized at high resolution. Initial stages of producing a website for the public viewing of the images were also carried out. Recently, the slides, digital images, and tissue have been transferred to Boston University for permanent archiving. A new steering committee has been established and plans are in place for completion of a freely accessible H.M. website. Research publications on the microscopic anatomy and neuropathology of H.M.'s brain at the time of his death are also planned. We write this commentary to provide the hippocampus and memory neuroscience communities with a brief summary of what has transpired following H.M.'s death and outline plans for future publications and a tissue archive.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 2","pages":"52-57"},"PeriodicalIF":3.5,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23597","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139377493","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}