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4. Evidence for an Evolutionarily Conserved Memory Coding Scheme in the Mammalian Hippocampus

Author

Thome, Alexander, Marrone, Diano F, Ellmore, Timothy M, Chawla, Monica K, Lipa, Peter, Ramirez-Amaya, Victor, Lisanby, Sarah H, McNaughton, Bruce L, and Barnes, Carol A

Subjects
Neurosciences, Behavioral and Social Science, Basic Behavioral and Social Science, 1.2 Psychological and socioeconomic processes, Underpinning research, 1.1 Normal biological development and functioning, Mental health, Neurological, Animals, Biological Evolution, Evidence-Based Medicine, Hippocampus, Macaca mulatta, Male, Memory, Episodic, Nerve Net, Orientation, Species Specificity, neural coding, neuroethology, primate, rodent, spatial cognition, virtual reality, Medical and Health Sciences, Psychology and Cognitive Sciences, Neurology & Neurosurgery
Abstract

Decades of research identify the hippocampal formation as central to memory storage and recall. Events are stored via distributed population codes, the parameters of which (e.g., sparsity and overlap) determine both storage capacity and fidelity. However, it remains unclear whether the parameters governing information storage are similar between species. Because episodic memories are rooted in the space in which they are experienced, the hippocampal response to navigation is often used as a proxy to study memory. Critically, recent studies in rodents that mimic the conditions typical of navigation studies in humans and nonhuman primates (i.e., virtual reality) show that reduced sensory input alters hippocampal representations of space. The goal of this study was to quantify this effect and determine whether there are commonalities in information storage across species. Using functional molecular imaging, we observe that navigation in virtual environments elicits activity in fewer CA1 neurons relative to real-world conditions. Conversely, comparable neuronal activity is observed in hippocampus region CA3 and the dentate gyrus under both conditions. Surprisingly, we also find evidence that the absolute number of neurons used to represent an experience is relatively stable between nonhuman primates and rodents. We propose that this convergence reflects an optimal ensemble size for episodic memories.SIGNIFICANCE STATEMENT One primary factor constraining memory capacity is the sparsity of the engram, the proportion of neurons that encode a single experience. Investigating sparsity in humans is hampered by the lack of single-cell resolution and differences in behavioral protocols. Sparsity can be quantified in freely moving rodents, but extrapolating these data to humans assumes that information storage is comparable across species and is robust to restraint-induced reduction in sensory input. Here, we test these assumptions and show that species differences in brain size build memory capacity without altering the structure of the data being stored. Furthermore, sparsity in most of the hippocampus is resilient to reduced sensory information. This information is vital to integrating animal data with human imaging navigation studies.

Published
2017

5. A biophysical minimal model to investigate age-related changes in CA1 pyramidal cell electrical activity.

Author

McKiernan, Erin C., Herrera-Valdez, Marco A., and Marrone, Diano F.

Subjects
PYRAMIDAL neurons, ION transport (Biology), OPEN-ended questions, MATHEMATICAL models, SIMPLICITY
Abstract

Aging is a physiological process that is still poorly understood, especially with respect to effects on the brain. There are open questions about aging that are difficult to answer with an experimental approach. Underlying challenges include the difficulty of recording in vivo single cell and network activity simultaneously with submillisecond resolution, and brain compensatory mechanisms triggered by genetic, pharmacologic, or behavioral manipulations. Mathematical modeling can help address some of these questions by allowing us to fix parameters that cannot be controlled experimentally and investigate neural activity under different conditions. We present a biophysical minimal model of CA1 pyramidal cells (PCs) based on general expressions for transmembrane ion transport derived from thermodynamical principles. The model allows directly varying the contribution of ion channels by changing their number. By analyzing the dynamics of the model, we find parameter ranges that reproduce the variability in electrical activity seen in PCs. In addition, increasing the L-type Ca2+ channel expression in the model reproduces age-related changes in electrical activity that are qualitatively and quantitatively similar to those observed in PCs from aged animals. We also make predictions about age-related changes in PC bursting activity that, to our knowledge, have not been reported previously. We conclude that the model's biophysical nature, flexibility, and computational simplicity make it a potentially powerful complement to experimental studies of aging. [ABSTRACT FROM AUTHOR]

Published
2024
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31. CA1 pyramidal cells have diverse biophysical properties, affected by development, experience, and aging

Author

McKiernan, Erin and Marrone, Diano F.

Abstract

This is a preprint. Feedback is welcome!AbstractNeuron types (e.g., pyramidal cells) within one area of the brain are often considered homogenous, despite variability in their biophysical properties. Here we review literature demonstrating variability in the electrical activity of CA1 hippocampal pyramidal cells (PCs), including responses to somatic current injection, synaptic stimulation, and spontaneous network-related activity. In addition, we describe how responses of CA1 PCs vary with development, experience, and aging, and some of the underlying ionic currents responsible. Finally, we suggest directions that may be the most impactful in expanding this knowledge, including the use of text and data mining to systematically study cellular heterogeneity in more depth; dynamical systems theory to understand and potentially classify neuron firing patterns; and mathematical modeling to study the interaction between cellular properties and network output. Our goals are to provide a synthesis of the literature for experimentalists studying CA1 PCs, to give theorists an idea of the rich diversity of behaviors models may need to reproduce to accurately represent these cells, and to provide suggestions for future research.

Published
2017
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38. Locus Coeruleus Phasic, But Not Tonic, Activation Initiates Global Remapping in a Familiar Environment.

Author

Grella, Stephanie L., Odintsova, Irina V., Marrone, Diano F., Neil, Jonathan M., Edison, Hilary T., Strong, Vanessa D., Walling, Susan G., Martin, Gerard M., and Harley, Carolyn W.

Abstract

Locus coeruleus (LC) neurons, the source of hippocampal norepinephrine (NE), are activated by novelty and changes in environmental contingencies. Based on the role of monoamines in reconfiguring invertebrate networks, and data from mammalian systems, a network reset hypothesis for the effects of LC activation has been proposed. We used the cellular compartmental analysis of temporal FISH technique based on the cellular distribution of immediate early genes to examine the effect of LC activation and inactivation, on regional hippocampal maps in male rats, when LC activity was manipulated just before placement in a second familiar (A/A) and/or novel environment (A/B). We found that bilateral phasic, but not tonic, activation of LC reset hippocampal maps in the A/A condition, whereas silencing the LC with clonidine before placement in the A/B condition blocked map reset and a familiar map emerged in the dentate gyrus, proximal and distal CA1, and CA3c. However, CA3a and CA3b encoded the novel environment. These results support a role for phasic LC responses in generating novel hippocampal sequences during memory encoding and, potentially, memory updating. The silencing experiments suggest that novel environments may not be recognized as different by dentate gyrus and CA1 without LC input. The functional distinction between phasic and tonic LC activity argues that these parameters are critical for determining network changes. These data are consistent with the hippocampus activating internal network representations to encode novel experiential episodes and suggest LC input is critical for this role. [ABSTRACT FROM AUTHOR]

Published
2019
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40. Attenuated Late-Phase Arc Transcription in the Dentate Gyrus of Mice Lacking Egr3.

Author

Maple, Amanda, Lackie, Rachel E., Elizalde, Diana I., Grella, Stephanie L., Damphousse, Chelsey C., Xa, Collin, Gallitano, Amelia L., and Marrone, Diano F.

Subjects
DENTATE gyrus, GENOTYPES, IN situ hybridization, LABORATORY mice, FLUORESCENCE
Abstract

The dentate gyrus (DG) engages in sustained Arc transcription for at least 8 hours following behavioral induction, and this time course may be functionally coupled to the unique role of the DG in hippocampus-dependent learning and memory. The factors that regulate long-term DG Arc expression, however, remain poorly understood. Animals lacking Egr3 show less Arc expression following convulsive stimulation, but the effect of Egr3 ablation on behaviorally induced Arc remains unknown. To address this, Egr3−/− and wild-type (WT) mice explored novel spatial environments and were sacrificed either immediately or after 5, 60, 240, or 480 minutes, and Arc expression was quantified by fluorescence in situ hybridization. Although short-term (i.e., within 60 min) Arc expression was equivalent across genotypes, DG Arc expression was selectively reduced at 240 and 480 minutes in mice lacking Egr3. These data demonstrate the involvement of Egr3 in regulating the late protein-dependent phase of Arc expression in the DG. [ABSTRACT FROM AUTHOR]

Published
2017
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41. Open Letter to The American Association for the Advancement of Science

Author

Tennant, Jonathan P, Poisot, Timothée, Kubke, M Fabiana, Michonneau, François, Taylor, Michael P, Steel, Graham, Anquetin, Jérémy, Coyte, Emily, Schwessinger, Benjamin, McKiernan, Erin C, Pollard, Tom, Eckert, Aimee, Allen, Liz, Chawla, Dalmeet Singh, Silva, Elizabeth, Gardner, Nicholas, Cantley, Nathan, Dupuis, John, Pikas, Christina, Buckland, Amy, Teytelman, Lenny, Faulkes, Zen, Gay, Robert J, Brett, Peter TB, Eklund, Anders, Björk, Johannes, Gunn, William, Desjardins-Proulx, Philippe, Nicholson, Joshua M, Edmunds, Scott, Ray Wilson, Steven, Buck, Stuart, Aksoy, B Arman, Fatima, Nazeefa, Mounce, Ross, Piwowar, Heather, Thirumalai, Avinash, Priem, Jason, Aldern, Clayton, Hanwell, Marcus D, Marhaver, Kristen L, Roberts, David Michael, Hole, Brian, Grossmann, Alexander, Vaux, David L, Murtagh, John, Carter, Alecia, Holcombe, Alex O, Aleman, Ignacio Torres, Molloy, Sarah, Lamp, John, Todd, Matthew, Seneviratne, Anusha, Guidotti, Guido, McArthur, Joseph, Grohmann, Carlos H, Leeuw, Jan de, Choi, Jung H, Priego, Ernesto, Pasley, Brian, Konkiel, Stacy, Hellen, Elizabeth HB, Levy, Raphael, Coxon, Paul, Pai, Nitika Pant, Carroll, David, Dávila, Jacinto, Herrera-Valdez, Marco Arieli, Alperin, Juan Pablo, de Ruiter, Jan P, Chen, Xianwen, Hatherill, Jeanette, Mullen, Katharine, Bekinschtein, Pedro, Groom, Quentin, Meijer-Kline, Karen, Gatti-Lafranconi, Pietro, Hollister, Jeffrey, Coin, Lachlan, Choi, MooYoung, Patterson-Lomba, Oscar, Ball, Rowena, Swan, Daniel, Curry, Stephen, Noyce, Abigail, Ward, Jordan, Meghreblian, Ben, White, Ethan P, Mulcahy, Sean R, Fausto, Sibele, Barba, Lorena A, Trollope, Ed, Beckett, Stephen, Steen, Andrew D, Sarv, Mari, Ross, Noam, Amir, Erika, Eve, Martin Paul, Cecchi, Franco, Colditz, Jason B, Spear, Philip, Menon, Mythili, Clapham, Matthew, Broman, Karl W, Triggs, Graham, Crick, Tom, Marrone, Diano F, Kraus, Joseph, Buyske, Steven, Simpson, Gavin, Morgan, Colleen, Woo, Kara, Tennant, Jonathan P, Poisot, Timothée, Kubke, M Fabiana, Michonneau, François, Taylor, Michael P, Steel, Graham, Anquetin, Jérémy, Coyte, Emily, Schwessinger, Benjamin, McKiernan, Erin C, Pollard, Tom, Eckert, Aimee, Allen, Liz, Chawla, Dalmeet Singh, Silva, Elizabeth, Gardner, Nicholas, Cantley, Nathan, Dupuis, John, Pikas, Christina, Buckland, Amy, Teytelman, Lenny, Faulkes, Zen, Gay, Robert J, Brett, Peter TB, Eklund, Anders, Björk, Johannes, Gunn, William, Desjardins-Proulx, Philippe, Nicholson, Joshua M, Edmunds, Scott, Ray Wilson, Steven, Buck, Stuart, Aksoy, B Arman, Fatima, Nazeefa, Mounce, Ross, Piwowar, Heather, Thirumalai, Avinash, Priem, Jason, Aldern, Clayton, Hanwell, Marcus D, Marhaver, Kristen L, Roberts, David Michael, Hole, Brian, Grossmann, Alexander, Vaux, David L, Murtagh, John, Carter, Alecia, Holcombe, Alex O, Aleman, Ignacio Torres, Molloy, Sarah, Lamp, John, Todd, Matthew, Seneviratne, Anusha, Guidotti, Guido, McArthur, Joseph, Grohmann, Carlos H, Leeuw, Jan de, Choi, Jung H, Priego, Ernesto, Pasley, Brian, Konkiel, Stacy, Hellen, Elizabeth HB, Levy, Raphael, Coxon, Paul, Pai, Nitika Pant, Carroll, David, Dávila, Jacinto, Herrera-Valdez, Marco Arieli, Alperin, Juan Pablo, de Ruiter, Jan P, Chen, Xianwen, Hatherill, Jeanette, Mullen, Katharine, Bekinschtein, Pedro, Groom, Quentin, Meijer-Kline, Karen, Gatti-Lafranconi, Pietro, Hollister, Jeffrey, Coin, Lachlan, Choi, MooYoung, Patterson-Lomba, Oscar, Ball, Rowena, Swan, Daniel, Curry, Stephen, Noyce, Abigail, Ward, Jordan, Meghreblian, Ben, White, Ethan P, Mulcahy, Sean R, Fausto, Sibele, Barba, Lorena A, Trollope, Ed, Beckett, Stephen, Steen, Andrew D, Sarv, Mari, Ross, Noam, Amir, Erika, Eve, Martin Paul, Cecchi, Franco, Colditz, Jason B, Spear, Philip, Menon, Mythili, Clapham, Matthew, Broman, Karl W, Triggs, Graham, Crick, Tom, Marrone, Diano F, Kraus, Joseph, Buyske, Steven, Simpson, Gavin, Morgan, Colleen, and Woo, Kara

Published
2014

43. Open Letter to The American Association for the Advancement of Science

Author

Tennant, Jonathan P., primary, Poisot, Timothée, additional, Kubke, M Fabiana, additional, Michonneau, François, additional, Taylor, Michael P., additional, Steel, Graham, additional, Anquetin, Jérémy, additional, Coyte, Emily, additional, Schwessinger, Benjamin, additional, McKiernan, Erin C., additional, Pollard, Tom, additional, Eckert, Aimee, additional, Allen, Liz, additional, Chawla, Dalmeet Singh, additional, Silva, Elizabeth, additional, Gardner, Nicholas, additional, Cantley, Nathan, additional, Dupuis, John, additional, Pikas, Christina, additional, Buckland, Amy, additional, Teytelman, Lenny, additional, Faulkes, Zen, additional, Gay, Robert J., additional, Brett, Peter T.B., additional, Eklund, Anders, additional, Björk, Johannes, additional, Gunn, William, additional, Desjardins-Proulx, Philippe, additional, Nicholson, Joshua M., additional, Edmunds, Scott, additional, Ray Wilson, Steven, additional, Buck, Stuart, additional, Aksoy, B. Arman, additional, Fatima, Nazeefa, additional, Mounce, Ross, additional, Piwowar, Heather, additional, Thirumalai, Avinash, additional, Priem, Jason, additional, Aldern, Clayton, additional, Hanwell, Marcus D., additional, Marhaver, Kristen L., additional, Roberts, David Michael, additional, Hole, Brian, additional, Grossmann, Alexander, additional, Vaux, David L., additional, Murtagh, John, additional, Carter, Alecia, additional, Holcombe, Alex O., additional, Aleman, Ignacio Torres, additional, Molloy, Sarah, additional, Lamp, John, additional, Todd, Matthew, additional, Seneviratne, Anusha, additional, Guidotti, Guido, additional, McArthur, Joseph, additional, Grohmann, Carlos H., additional, Leeuw, Jan de, additional, Choi, Jung H., additional, Priego, Ernesto, additional, Pasley, Brian, additional, Konkiel, Stacy, additional, Hellen, Elizabeth HB, additional, Levy, Raphael, additional, Coxon, Paul, additional, Pai, Nitika Pant, additional, Carroll, David, additional, Dávila, Jacinto, additional, Herrera-Valdez, Marco Arieli, additional, Alperin, Juan Pablo, additional, de Ruiter, Jan P., additional, Chen, Xianwen, additional, Hatherill, Jeanette, additional, Mullen, Katharine, additional, Bekinschtein, Pedro, additional, Groom, Quentin, additional, Meijer-Kline, Karen, additional, Gatti-Lafranconi, Pietro, additional, Hollister, Jeffrey, additional, Coin, Lachlan, additional, Choi, MooYoung, additional, Patterson-Lomba, Oscar, additional, Ball, Rowena, additional, Swan, Daniel, additional, Curry, Stephen, additional, Noyce, Abigail, additional, Ward, Jordan, additional, Meghreblian, Ben, additional, White, Ethan P., additional, Mulcahy, Sean R., additional, Fausto, Sibele, additional, Barba, Lorena A., additional, Trollope, Ed, additional, Beckett, Stephen, additional, Steen, Andrew D., additional, Sarv, Mari, additional, Ross, Noam, additional, Amir, Erika, additional, Eve, Martin Paul, additional, Cecchi, Franco, additional, Colditz, Jason B., additional, Spear, Philip, additional, Menon, Mythili, additional, Clapham, Matthew, additional, Broman, Karl W., additional, Triggs, Graham, additional, Crick, Tom, additional, Marrone, Diano F., additional, Kraus, Joseph, additional, Buyske, Steven, additional, Simpson, Gavin, additional, Morgan, Colleen, additional, and Woo, Kara, additional

Published
2014
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44. Open letter to the Society for Neuroscience

Author

McKiernan, Erin C., primary, Herrera-Valdez, Marco Arieli, additional, Madan, Christopher R., additional, Desjardins-Proulx, Philippe, additional, Eklund, Anders, additional, Kubke, M Fabiana, additional, Holcombe, Alex O., additional, Steel, Graham, additional, Marrone, Diano F., additional, Oppenheim, Charles, additional, Faulkes, Zen, additional, Tennant, Jonathan P., additional, Gardner, Nicholas M., additional, Thirumalai, Avinash, additional, Park, Travis, additional, Meghreblian, Ben, additional, Kaplan, Sean, additional, Chambers, Chris, additional, Nicholson, Joshua M., additional, Velterop, Jan, additional, Poisot, Timothée, additional, Anquetin, Jérémy, additional, Allen, Liz Allen, additional, Björk, Johannes, additional, Mounce, Ross, additional, Edmunds, Scott, additional, Cruz-Aponte, Maytée, additional, Hancock, Joseph R., additional, Fatima, Nazeefa, additional, Pant Pai, Nitika, additional, Silva, Elizabeth, additional, Brembs, Björn, additional, Ridgway, Gerard, additional, Gatti-Lafranconi, Pietro, additional, Chen, Xianwen, additional, Dávila, Jacinto, additional, de Bivort, Benjamin, additional, Beckett, Stephen, additional, Menon, Mythili, additional, Choraziak, Adam, additional, Triggs, Graham, additional, Dumas, Guillaume, additional, Hollister, Jeffrey W., additional, Gruson-Daniel, Célya, additional, McDowell, Gary S., additional, Klein, Pierre-Alexandre, additional, Laroche, Julien, additional, Thome, Alex, additional, Guyon, Nicolas, additional, Fausto, Sibele, additional, Finlayson, Nonie, additional, Singh Chawla, Dalmeet, additional, Wilbanks, John, additional, Carroll, David, additional, Martínez-Molina, Noelia, additional, Sloan, Maximilian, additional, and Eglen, Stephen, additional

Published
2014
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