Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning

Click to view the published version. Jump to navigation Jump to search This article is about the section in the sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. For the fish genus Hippocampus, see Seahorse.

In rodents as model organisms, the hippocampus has been studied extensively as part of a brain system responsible for spatial memory and navigation. Since different neuronal cell types are neatly organized into layers in the hippocampus, it has frequently been used as a model system for studying neurophysiology. The hippocampus can be seen as a ridge of gray matter tissue, elevating from the floor of each lateral ventricle in the region of the inferior or temporal horn. The term hippocampal formation is used to refer to the hippocampus proper and its related parts. However, there is no consensus as to what parts are included. Sometimes the hippocampus is said to include the dentate gyrus and the subiculum.

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In a cross-section of the hippocampus, including the dentate gyrus, several layers will be shown. The layers are from the outer in – the molecular layer, the inner molecular layer, the granular layer, and the hilus. The CA3 in the hippocampus proper has the following cell layers known as strata: lacunosum-moleculare, radiatum, lucidum, pyramidal, and oriens. The EC, is located in the parahippocampal gyrus, a cortical region adjacent to the hippocampus. Image 4: Basic circuit of the hippocampus, as drawn by Cajal DG: dentate gyrus.

The flow of information in the hippocampus is largely unidirectional. Some axons project to CA3 and a lesser number project to CA1. Basket cells in CA3 receive excitatory input from the pyramidal cells and then give an inhibitory feedback to the pyramidal cells. This recurrent inhibition is a simple feedback circuit that can dampen excitatory responses in the hippocampus. Several other connections play important roles in hippocampal function. Beyond the output to the EC, additional output pathways go to other cortical areas including the prefrontal cortex.

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Areas of the hippocampus are shown to be functionally and anatomically distinct. The dorsal hippocampus serves for spatial memory, verbal memory, and learning of conceptual information. The intermediate hippocampus has overlapping characteristics with both the ventral and dorsal hippocampus. Over the years, three main ideas of hippocampal function have dominated the literature: response inhibition, episodic memory, and spatial cognition. The second major line of thought relates the hippocampus to memory.

The third important theory of hippocampal function relates the hippocampus to space. The spatial theory was originally championed by O’Keefe and Nadel, who were influenced by E. Tolman’s theories about “cognitive maps” in humans and animals. Later research has focused on trying to bridge the disconnect between the two main views of hippocampal function as being split between memory and spatial cognition. In some studies, these areas have been expanded to the point of near convergence.

It has also been proposed that the spiking activity of hippocampal neurons is associated spatially, and it was suggested that the mechanisms of memory and planning both evolved from mechanisms of navigation and that their neuronal algorithms were basically the same. The anterior hippocampus is seen to be involved in decision-making under approach-avoidance conflict processing. Due to bilateral symmetry the brain has a hippocampus in each cerebral hemisphere. If damage to the hippocampus occurs in only one hemisphere, leaving the structure intact in the other hemisphere, the brain can retain near-normal memory functioning. Furthermore, amnesic patients frequently show “implicit” memory for experiences even in the absence of conscious knowledge. Image 6: Spatial firing patterns of 8 place cells recorded from the CA1 layer of a rat.

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The rat ran back and forth along an elevated track, stopping at each end to eat a small food reward. Dots indicate positions where action potentials were recorded, with color indicating which neuron emitted that action potential. Studies on freely moving rats and mice have shown many hippocampal neurons to act as place cells that cluster in place fields, and these fire bursts of action potentials when the animal passes through a particular location. In humans, cells with location-specific firing patterns have been reported during a study of patients with drug-resistant epilepsy. They were undergoing an invasive procedure to localize the source of their seizures, with a view to surgical resection. There are several navigational cells in the brain that are either in the hippocampus itself or are strongly connected to it, such as the speed cells present in the medial entorhinal cortex.

Together these cells form a network that serves as spatial memory. Approach-avoidance conflict happens when a situation is presented that can either be rewarding or punishing, and the ensuing decision-making has been associated with anxiety. A review makes reference to a number of studies that show the involvement of the hippocampus in conflict tasks. The authors suggest that a challenge is to understand how conflict processing relates to the functions of spatial navigation and memory and how all of these functions need not be mutually exclusive.

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The top plot represents a time period during which the rat was actively searching for scattered food pellets. These two hippocampal activity modes can be seen in primates as well as rats, with the exception that it has been difficult to see robust theta rhythmicity in the primate hippocampus. There are, however, qualitatively similar sharp waves and similar state-dependent changes in neural population activity. Because of its densely packed neural layers, of all the brain structures which generate the hippocampal theta rhythm, the hippocampus generates some of the largest EEG signals as theta waves . In some situations the EEG is dominated by regular waves at 3 to 10 Hz, often continuing for many seconds.

Theta rhythmicity is very obvious in rabbits and rodents and also clearly present in cats and dogs. Whether theta can be seen in primates is not yet clear. During sleep or during resting, when an animal is not engaged with its surroundings, the hippocampal EEG shows a pattern of irregular slow waves, somewhat larger in amplitude than theta waves. This pattern is occasionally interrupted by large surges called sharp waves. These events are associated with bursts of spike activity lasting 50 to 100 milliseconds in pyramidal cells of CA3 and CA1.

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One of the most interesting aspects of sharp waves is that they appear to be associated with memory. The hippocampus is a particularly favorable site for studying LTP because of its densely packed and sharply defined layers of neurons, but similar types of activity-dependent synaptic change have also been observed in many other brain areas. The hippocampus contains high levels of glucocorticoid receptors, which make it more vulnerable to long-term stress than most other brain areas. Chronic stress resulting in elevated levels of glucocorticoids, notably of cortisol, is seen to be a cause of neuronal atrophy in the hippocampus.

This atrophy results in a smaller hippocampal volume which is also seen in Cushing’s syndrome. The higher levels of cortisol in Cushing’s syndrome is usually the result of medications taken for other conditions. Sex-specific responses to stress have also been demonstrated in the rat to have an effect on the hippocampus. Chronic stress in the male rat showed dendritic retraction and cell loss in the CA3 region but this was not shown in the female. This was thought to be due to neuroprotective ovarian hormones. The hippocampus is one of the few brain regions where new neurons are generated. This process of neurogenesis is confined to the dentate gyrus.

The production of new neurons can be positively affected by exercise or negatively affected by epileptic seizures. Seizures in temporal lobe epilepsy can affect the normal development of new neurons and can cause tissue damage. Hippocampal sclerosis is the most common type of such tissue damage. The causes of schizophrenia are not well understood, but numerous abnormalities of brain structure have been reported. The most thoroughly investigated alterations involve the cerebral cortex, but effects on the hippocampus have also been described. Many reports have found reductions in the size of the hippocampus in schizophrenic subjects.

The hippocampus has been seen as central to the pathology of schizophrenia, both in the neural and physiological effects. It has been generally accepted that there is an abnormal synaptic connectivity underlying schizophrenia. Transient global amnesia is a dramatic, sudden, temporary, near-total loss of short-term memory. There has been no scientific proof of any cause.

24 hours following an episode has shown there to be small dot-like lesions in the hippocampus. These findings have suggested a possible implication of CA1 neurons made vulnerable by metabolic stress. The hippocampus has a generally similar appearance across the range of mammals, from monotremes such as the echidna to primates such as humans. The hippocampal-size-to-body-size ratio broadly increases, being about twice as large for primates as for the echidna.

There is also a general relationship between the size of the hippocampus and spatial memory. When comparisons are made between similar species, those that have a greater capacity for spatial memory tend to have larger hippocampal volumes. Non-mammalian species do not have a brain structure that looks like the mammalian hippocampus, but they have one that is considered homologous to it. The hippocampus, as pointed out above, is in essence part of the allocortex. In birds, the correspondence is sufficiently well established that most anatomists refer to the medial pallial zone as the “avian hippocampus”. Numerous species of birds have strong spatial skills, in particular those that cache food. There is evidence that food-caching birds have a larger hippocampus than other types of birds and that damage to the hippocampus causes impairments in spatial memory.

The story for fish is more complex. Most neuroanatomists believe that the teleost forebrain is in essence everted, like a sock turned inside-out, so that structures that lie in the interior, next to the ventricles, for most vertebrates, are found on the outside in teleost fish, and vice versa. It is not yet known whether the medial pallium plays a similar role in even more primitive vertebrates, such as sharks and rays, or even lampreys and hagfish. Lymbic system and cerebral circuits for emotions, learning, and memory”. In Anderson P, Morris R, Amaral, Bliss T, O’Keefe J. Hippocampus minor, calcar avis, and the Huxley-Owen debate”. The limbic system conception and its historical evolution”.

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Department of Neurobiology and Anatomy – The University of Texas Medical School at Houston”. Archived from the original on 2013-12-03. Defining and controlling the circuits of emotion”. Origins of neuroscience: a history of explorations into brain function.

Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections”. Memory and Space: Towards an Understanding of the Cognitive Map”. The hippocampus and declarative memory: Cognitive mechanisms and neural codes”. Memory, navigation and theta rhythm in the hippocampal-entorhinal system”. The role of the hippocampus in approach-avoidance conflict decision-making: Evidence from rodent and human studies”. Learning and Memory From Brain to Behavior Second Edition. Severe amnesia following bilateral medial temporal lobe damage occurring on two distinct occasions”.

Primary CA1 and conditionally immortal MHP36 cell grafts restore conditional discrimination learning and recall in marmosets after excitotoxic lesions of the hippocampal CA1 field”. Phase relationship between hippocampal place units and the EEG theta rhythm”. Pattern of hippocampal shape and volume differences in blind subjects”. Examining the Role of the Human Hippocampus in Approach-Avoidance Decision Making Using a Novel Conflict Paradigm and Multivariate Functional Magnetic Resonance Imaging”. Synchrony between limbic system theta activity and rhythmical behavior in rats”.

Journal of comparative and physiological psychology. Selective suppression of hippocampal ripples impairs spatial memory”. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat”. Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus”. A meta-analysis of structural brain abnormalities in PTSD”.

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Meta-analysis of regional brain volumes in schizophrenia”. Structural neuroimaging studies in major depressive disorder. Meta-analysis and comparison with bipolar disorder”. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing’s disease”. Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis”. Cholesterol and perhaps estradiol protect against corticosterone-induced hippocampal CA3 dendritic retraction in gonadectomized female and male rats”.

Verbal learning and hippocampal dysfunction in schizophrenia: A meta-analysis. Click to view the published version. Jump to navigation Jump to search This article is about the section in the brain. For the fish genus Hippocampus, see Seahorse. In rodents as model organisms, the hippocampus has been studied extensively as part of a brain system responsible for spatial memory and navigation.

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Since different neuronal cell types are neatly organized into layers in the hippocampus, it has frequently been used as a model system for studying neurophysiology. The hippocampus can be seen as a ridge of gray matter tissue, elevating from the floor of each lateral ventricle in the region of the inferior or temporal horn. The term hippocampal formation is used to refer to the hippocampus proper and its related parts. However, there is no consensus as to what parts are included.

Sometimes the hippocampus is said to include the dentate gyrus and the subiculum. In a cross-section of the hippocampus, including the dentate gyrus, several layers will be shown. The layers are from the outer in – the molecular layer, the inner molecular layer, the granular layer, and the hilus. The CA3 in the hippocampus proper has the following cell layers known as strata: lacunosum-moleculare, radiatum, lucidum, pyramidal, and oriens.

The EC, is located in the parahippocampal gyrus, a cortical region adjacent to the hippocampus. Image 4: Basic circuit of the hippocampus, as drawn by Cajal DG: dentate gyrus. The flow of information in the hippocampus is largely unidirectional. Some axons project to CA3 and a lesser number project to CA1. Basket cells in CA3 receive excitatory input from the pyramidal cells and then give an inhibitory feedback to the pyramidal cells. This recurrent inhibition is a simple feedback circuit that can dampen excitatory responses in the hippocampus.