Dynamic Hippocampal Circuits Support Learning- and Memory-Guided Behaviors

Anderson, Emily B.; Grossrubatscher, Irene; Frank, Loren M.

doi:10.1101/sqb.2014.79.024760

Cited by 14 publications

(11 citation statements)

References 64 publications

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“…In the first, developmentally specified neural circuits generate rapid innate responses to sensory stimuli that have remained relatively constant and predictable over evolutionary timescales (1)(2)(3)(4)(5). In the second, neural circuits generate flexible responses to stimuli that can change over an individual's lifespan, through learning and memory (6)(7)(8).…”

Section: Introductionmentioning

confidence: 99%

Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP

Stagkourakis

Spigolon

Liu

et al. 2020

Preprint

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All animals can perform certain survival behaviors without prior experience, suggesting a “hard wiring” of underlying neural circuits. Experience, however, can alter the expression of innate behaviors. Where in the brain and how such plasticity occurs remains largely unknown. Previous studies have established the phenomenon of “aggression training,” in which the repeated experience of winning successive aggressive encounters across multiple days leads to increased aggressiveness. Here we show that this procedure also leads to long-term potentiation (LTP) at an excitatory synapse, derived from the Anterior Hippocampus/Posterior Medial amygdala (AHiPM), onto estrogen receptor 1-expressing (Esr1+) neurons in the ventrolateral subdivision of the ventromedial hypothalamus (VMHvl). We demonstrate further that the optogenetic induction of such LTP in vivo facilitates, while optogenetic long-term depression (LTD) diminishes, the behavioral effect of aggression training, implying a causal role for potentiation at AHiPM➔VMHvlEsr1 synapses in mediating the effect of this training. Interestingly, ∼25% of inbred C57BL/6 mice fail to respond to aggression training. We show that these individual differences are correlated both with lower levels of testosterone, relative to mice that respond to such training, and with a failure to exhibit LTP in vivo after aggression training. Administration of exogenous testosterone to such non-aggressive mice restores both behavioral and physiological plasticity in vivo. Together, these findings reveal that LTP at a hypothalamic circuit node mediates a form of experience-dependent plasticity in an innate social behavior, and a potential hormone-dependent basis for individual differences in such plasticity among genetically identical mice.Significance StatementModification of instinctive behaviors occurs through experience, yet the mechanisms through which this happens have remained largely unknown. Recent studies have shown that potentiation of aggression, an innate behavior, can occur through repeated winning of aggressive encounters. Here we show that synaptic plasticity at a specific excitatory input to a hypothalamic cell population is correlated with, and required for, the expression of increasingly higher levels of aggressive behavior following successful aggressive experience. We additionally show that the amplitude and persistence of long-term potentiation at this synapse are influenced by serum testosterone, administration of which can normalize individual differences among genetically identical inbred mice, in the expression of intermale aggression.

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Section: Introductionmentioning

confidence: 99%

Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP

Stagkourakis

Spigolon

Liu

et al. 2020

Preprint

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“…The hippocampus provides an ideal structure to consider functional cellular heterogeneity, given the abundance of data available from this area, as well as its critical role in learning and memory ( Anderson, Grossrubatscher & Frank, 2014 ; Preston & Eichenbaum, 2013 ; Buzsáki & Moser, 2013 ; Yassa et al, 2011 ; Yassa & Stark, 2011 ). Hippocampal pyramidal cells (PCs) have been studied extensively using a variety of stimulation protocols and tasks ( Spruston, 2008 ; Disterhoft, Wu & Ohno, 2004 ; Wiener, 1996 ).…”

Section: Introductionmentioning

confidence: 99%

CA1 pyramidal cells have diverse biophysical properties, affected by development, experience, and aging

McKiernan

Marrone

2017

PeerJ

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Neuron types (e.g., pyramidal cells) within one area of the brain are often considered homogeneous, 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.

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“…The hippocampus also plays a crucial role in long-term memory consolidation [97] and learning [32,98]. Working memory has been shown several times to improve with yoga practice [45,99,100].…”

Section: -Week Hatha Yoga Increases Right Hippocampal Density Compamentioning

confidence: 99%

10-Week Hatha Yoga Increases Right Hippocampal Density Compared to Active and Passive Control Groups: A Controlled Structural cMRI Study

Garner¹,

Reith²,

Krick³

2019

J Neuroimaging Psychiatry Neurol

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Background:The current study was designed to evaluate potential Yoga specific changes of brain structure in comparison with an active sport group and a passive control group. Materials and Methods:We conducted a longitudinal structural MRI study to investigate changes in gray matter (GM) density following a Yoga intervention. In order to check the repeatability of the results two data acquisition periods (cohorts) with the same study design were done. Yoga naive subjects (n = 19/n = 20) received a Yoga intervention once a week for 75 minutes over a period of 10 weeks. Control groups included active sport subjects (n = 10/n = 22) and passive subjects (n = 17/n = 14). All participants could choose their group assignment by their own preference. A longitudinal and group comparison was done by voxelbased-morphometric analyses before and after the intervention. In addition, blood pressure was taken before and after the study period as a controlling instrument. Finally, the results of the two cohorts were reported into a comprising data set for a general conclusion on Yoga effects. Results:Initially, hippocampal GM density in the Yoga group was significantly lower than in both control groups already before the intervention. It was equally and independently present in both cohorts. The longitudinal MRI measurements showed a significant increase in the right hippocampal GM density as a specific effect of the Hatha Yoga intervention. Coincidentally, the blood pressure measurement detected a significant reduction in both systolic and diastolic blood pressure in the Yoga group but not in the sport or passive group. Conclusions:Various neurodegenerative and neuropsychiatric diseases as well as long lasting stress lead to structural shrinkage of the hippocampal GM. In contrast, stress reduction was shown to be associated with an increase in the hippocampal GM density. The Yoga specific effect in this study can be considered as positive impact on both stress management and its underlying neural structure. These effects have been already proven in prevention and therapy of neurodegenerative and neuropsychiatric diseases. The Yoga-induced stress reduction can be furthermore supported by the findings of blood pressure reduction. Blood pressure is well known as an indirect indicator for stress reduction. Since the GM density was detected lower in the two Yoga cohorts twice compared to both control groups, one may postulate a pre-existing but unconscious higher stress vulnerability when voluntarily deciding for the Yoga intervention.

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Dynamic Hippocampal Circuits Support Learning- and Memory-Guided Behaviors

Cited by 14 publications

References 64 publications

Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP

Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP

CA1 pyramidal cells have diverse biophysical properties, affected by development, experience, and aging

10-Week Hatha Yoga Increases Right Hippocampal Density Compared to Active and Passive Control Groups: A Controlled Structural cMRI Study

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