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WIREs Cogn Sci
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Hippocampus

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Abstract Damage to the hippocampus and related brain regions causes a profound amnesic syndrome, in which patients are unable to form new memories about their experiences and about facts about the world. A number of theories have been proposed to explain hippocampal function. The theories that are currently most influential propose that the hippocampus is the substrate of declarative or episodic memory and that the hippocampus is the neural locus of a cognitive map. Anatomical, physiological, and behavioral studies of the hippocampal system have enabled a rich understanding of a number of general principles of information processing and storage in the brain. In this article, we describe key anatomical and physiological features of hippocampal function as well as the most influential theories of hippocampal function. WIREs Cogn Sci 2012, 3:231–251. doi: 10.1002/wcs.1164 This article is categorized under: Neuroscience > Cognition

Hippocampus anatomy. (a) Position of the hippocampus in the rat brain. The drawing depicts a rat brain after the neocortex overlying the hippocampus was removed to reveal the position and the shape of hippocampus. S: septal pole of hippocampus; T: temporal pole; TRANS: transverse axis, orthogonal to the septotemporal axis. Inset shows enlargement of a section along the transverse axis, with the ‘trisynaptic pathway’.6 CA1, CA3: areas CA1 and CA3 of the hippocampus, DG: dentate gyrus, mf: mossy fibers, pp: perforant path, S: subiculum, sc: Schaffer collaterals. (Reprinted with permission from Ref 7. Copyright 1989 Elsevier Limited) (b) Nissl stained coronal section of the rat brain showing the hippocampus. CA1, CA2, CA3: areas CA1, CA2, and CA3 of the hippocampus; DG: dentate gyrus; G: granule cell layer of the dentate gyrus; l: stratum lucidum of CA3; l‐m: stratum lacunosum‐moleculare; m: molecular layer of DG; o: stratum oriens; p: pyramidal cell layer; pl: polymorphic layer of DG, also referred to as the hilus; r: stratum radiatum. (c) Nissl stained coronal section of the rat brain showing medial (MEC) and lateral (LEC) entorhinal cortex. Layers I–VI are marked.

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Classification of memory.117

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Long term potentiation (LTP) and depression (LTD). (a) Schematic showing excitatory postsynaptic potentials (EPSPs) recorded in response to electrical stimulation of the presynaptic axons. The waveforms show a stimulation artefact corresponding to the test stimulus applied to the presynaptic axons followed by EPSPs. The gray line shows baseline EPSP recorded before induction of LTP or LTD, while the black lines show the changed amplitude of EPSP after induction. LTP induction protocols give rise to a larger EPSP amplitude (potentiation), while LTD induction protocols give rise to a smaller EPSP amplitude (depression). These changes last for prolonged periods of time (hours to days). (b) and (c) Schematics showing EPSP amplitude as a function of time. Arrowheads indicate timing of LTP inducing stimuli in (b) and LTD inducing stimuli in (c). Low frequency stimuli used in LTD induction typically last a few minutes, and hence there is a temporal gap between the pre‐ and post‐stimulus amplitudes in (c).

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Temporal ordering of place cells during behavior and ripples. (a) Schematic showing the relative timing of firing of place cells with partially overlapping place fields on a linear track. LFP theta oscillations are shown on top, and spikes of different neurons in different colors are shown below. Theta phase precession organizes the firing of neurons such that neurons with place field centers earlier in the rat's trajectory fire earlier within the theta cycle than the neurons with place field centers later in the rat's trajectory. This ensures that neurons maintain similar relative timing of firing over multiple theta cycles.87 (b) and (c) Sharp waves (b) and ripples (c) are observed during awake immobility or slow wave sleep after the behavior. During these sharp wave–ripple epochs, a large number of CA1 and CA3 neurons tend to fire. Their order of firing within a ripple event tends to replay the order observed during the preceding behavior session.

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Theta phase locking and theta phase precession. (a) Schematic showing theta oscillations in the LFP, and simultaneously recorded spikes of theta phase locking (red) and theta phase precessing (cyan) neurons while the rat runs on a linear track. Vertical lines mark locations of valleys in the LFP oscillations, for ease of identifying the phase of the theta cycle when the neurons fired. (b) Distribution of theta phase at which the two neurons fire as a function of position. The red neuron fires in approximately the same phase of theta in each cycle, while the cyan neuron fires in earlier and earlier phases of theta as the rat traverses through the place field of this neuron. Data from multiple runs on a linear track are used to generate phase precession plots like this. Hippocampal place cells show theta phase precession, while interneurons tend to show theta phase locking.

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Local field potentials show different patterns corresponding to different behavioral states. (a) Large irregular activity seen during immobility, slow‐wave sleep, and nonexploratory behaviors. Two of the sharp waves observed during this epoch are marked. (b) High frequency ripples recorded simultaneously as the trace in (a), from an electrode in the CA1 pyramidal cell layer, where the ripple amplitude is strongest. (c) Theta oscillations observed during locomotion. Bandpass frequencies for each of the three traces are shown at the upper right corner of each trace.

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Grid cells. (a) Firing rate map of a simulated grid cell. See Figure 5 for explanation of how a firing rate map is generated. The grid cell fires when the rat is at regularly spaced vertices of a tessellating grid of equilateral triangles. (b) Neighboring grid cells fire at locations offset from each other, while maintaining a similar inter‐vertex spacing and orientation. The 3 colors represent the vertices of three different grid cells. (c) Grid cells recorded from the part of MEC more ventral than the grids cells shown in (b). Notice how both the inter‐vertex spacing as well as the size of the vertices is larger than those in (b).

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Head direction cells. The plots show schematic representations of the firing rates of three head direction cells as a function of the direction of the rat's head. Each head direction cell has a preferred head direction at which it maximally fires, and the preferred directions of the head direction cell population cover the entire 360° range.

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Place cells. The five squares represent the 5 ft2 box in which the rat was foraging, with the pattern of activity (firing rate map) of each of the five simultaneously recorded place cells (units) shown in one square each. Colors represent the firing rates of the neurons in different locations in the box, with a firing rate of 0 Hz represented by blue and the highest firing rate for the given neuron represented by red. Notice that the five neurons have different preferred firing locations within the box.

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Complex spike in the hippocampus. Extracellular recordings of action potentials from a cell recorded in vivo are shown here. Negative is up. Notice how the amplitude of the action potential drops during a burst, while the interspike interval remains around 3 ms. The number of spikes during a burst is variable.

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Segregation of projections to hippocampus along the proximal‐distal and septo‐temporal axes. (a) Schematic showing segregation of inputs to proximal and distal portions of CA1 and subiculum. Arrowheads represent the direction of information flow. Note that LEC and MEC also project directly to all parts of the DG and CA3 regions, but these connections are omitted for simplicity. (b). Schematic showing topographical projection of LEC and MEC inputs to the hippocampus. The lateral (L) part of LEC (near the rhinal sulcus) and the dorsocaudal (DC) part of MEC project to the septal (S) region of the hippocampus (HC), while the medial (M) part of LEC and the ventral (V) part of MEC project to the temporal (T) region of the hippocampus.

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Information flow in the hippocampal formation. LEC receives major input from perirhinal cortex, which is part of the ventral ‘what’ pathway, while MEC receives major input from postrhinal (parahippocampal) cortex. The projections from LEC and MEC layer III to CA1 and subiculum remain segregated along the transverse (proximal‐distal) axis of the hippocampus, whereas the projections from LEC and MEC layer II to the DG and CA3 converge onto the same anatomical regions. See text for details.

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