1. Chapter 19 The adult hippocampal network
From Cellular and Molecular Neurophysiology, Fourth Edition.
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2. Figure 19.1 Schematic of the localization of the two hippocampi inside a rat brain.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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3. Figure 19.2 Structure of the rat hippocampus.
(a) Schematic of the slice preparation protocol. (b) Schematic transverse section of the hippocampus. ALV: stratum alveus, OR: stratum oriens, P: stratum pyramidale, RAD: stratum radiatum, LAC-MOL: stratum lacunosum moleculare, MOL: stratum moleculare.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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4. Figure 19.3 Extracellular field recordings of hippocampal oscillations in a freely moving rat during transition from walking to immobility.
An extracellular recording electrode is implanted in the stratum radiatum (RAD) of the CA1 region of each hippocampus, the left (L) and the right (R). During exploratory activity (walking), regular theta waves are recorded (θ); during immobility, large monophasic sharp waves (SPW) are recorded. Note the bilaterally synchronous nature of SPW. Sch: Schaffer collaterals, i.e. axons of CA3 pyramidal cells.
Adapted from Buzsáki G (1989) Two-stage model of memory trace formation: a role for ‘noisy’ brain states. Neuroscience31, 551–570, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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5. Figure 19.4 Photomicrographs of stained Golgi CA1 and CA3 pyramidal neurons and CA1 interneurons.
(a) CA1 pyramidal neuron. (b) CA3 pyramidal neuron. The underlying Nissl coloration shows the density of neuronal cell bodies in the pyramidal layer. The arrow points to the giant dendritic spines. (c,d) Examples of CA1 GABAergic interneurons labeled with GFP. Their cell body is located inside or close to the pyramidal cell layer (P). The thin labeling corresponds to axon and axon collaterals. Scales: 50 μm in a–d. Photographs: (a) by Olivier Robain; (b) by Jean Luc Gaiarsa; (c,d) by Agnès Baude.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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6. Figure 19.5 Intrinsic connections in CA1 and CA3.
(a) Schematic of a pyramidal cell indicating the localization of the cell bodies of the different interneurons (left) and the segregated postsynaptic domains innervated by the distinct presynaptic interneurons (right). (b) Illustration of feedforward and feedback inhibition. See text for abbreviations.
Part (a) adapted from Maccaferri G, Roberts DB, Szucs P et al. (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol. 524, 91–116, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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7. 7 Figure 19.6 The tri-neuronal circuit between principal cells.
(a) Sites of termination of axons of principal cells on target principal cells (which are CA1 and CA3 pyramidal cells). Axons of granular cells are called mossy fibers. Axonal collaterals of CA3 pyramidal cells are called Schaffer collaterals. (b) The tri-neuronal circuit is organized in the transverse plane. LUC, stratum lucidum of CA3; pyr cell, pyramidal cell. (c) Illustration of recurrent excitation.
Part (a) adapted from Altman J, Brunner RL, Bayer SA (1973) The hippocampus and behavioral maturation. Behav. Biol. 8, 557–596, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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8. Figure 19.7 Schematic of the synaptic circuitry in the CA1 region of the hippocampus and afferent connections from Schaffer collaterals of CA3 pyramidal cells.
Adapted from Altman J, Brunner RL, Bayer SA (1973) The hippocampus and behavioural maturation. Behav. Biol.8, 557–596, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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9. 9 From Cellular and Molecular Neurophysiology, Fourth Edition.
Figure 19.8 Physiological characteristics that differentiate pyramidal neurons from interneurons.
(a) Action potential of a pyramidal neuron at a fast (1) and a slow (2) time base to show the presence of an after-spike depolarization (arrow) followed by a slow after-spike hyperpolarization (double arrow). The bottom trace (3) shows the response of a pyramidal neuron to a depolarizing current pulse. (b) Action potential of an interneuron recorded in the stratum oriens (OR) at a fast (1) and a slow (2) time base to show the presence of a fast after-spike-hyperpolarization (arrow). The bottom trace (3) shows the response of a pyramidal neuron (a) or an interneuron (b) to a depolarizing current pulse applied via the recording whole cell electrode.
Adapted from Lacaille JC, Williams S (1990) Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience36, 349–359, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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10. Figure 19.9 Unitary IPSCs (uIPSCs) evoked in pyramidal cells in response to different types of interneurons are all mediated by GABAA receptors.
Averaged uIPSC evoked in a pyramidal neuron (2) in response to a single spike in a bistratified interneuron (1a, BiC) or an oriens lacunosum moleculare interneuron (1b, O-LMC) in control conditions, in the presence of bicuculline (Bicu, 10 μ M) and after partial washout of the drug (Wash).
Adapted from Maccaferri G, Roberts DB, Szucs P et al. (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol.524, 91–116, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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11. Figure Kinetic parameters of unitary IPSCs evoked in a pyramidal cell in response to different types of interneurons.
(a) Definition of the parameters of postsynaptic currents. (b) Comparison of the risetime (or time to peak) and decay phase of three different uIPSCs. The decay phase of the uIPSC generated by an O-LM cell is fitted by an exponential (black trace) to obtain the value of τ. Bottom trace shows superimposed averaged uIPSCs generated by a presynaptic basket cell (BC) or oriens lacunosum moleculare cell (O-LMC) and scaled at the same amplitude. Note the much longer time to peak of the IPSC evoked by the O-LM cell in comparison with that of the basket cell. (c) Histogram of the risetimes (10–90%) and (d) of the decay (τ, time to 63% of decay) of the uIPSCs generated by different classes of presynaptic interneurons.
Adapted from Maccaferri G, Roberts DB, Szucs P et al. (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J. Physiol. 524, 91–116, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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12. Figure 19.11 Unitary IPSP evoked in a CA1 pyramidal cell in response to a bistratified cell (BiC).
(a) Reconstruction of the biocytin-filled presynaptic interneuron (somato-dendritic tree in blue, axon in yellow) and a postsynaptic pyramidal cell (green). (b) An action potential in BiC (1) elicits a small-amplitude, short-latency unitary IPSP in the postsynaptic pyramidal cell (2). (Trace 2 is an averaged unitary IPSP.)
Adapted from Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature368, 823–828, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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13. Figure Unitary IPSP evoked in a granular cell in response to an axo-axonic cell (AAC) and location of contact sites.
(a) Reconstruction of the biocytin-filled presynaptic interneuron (soma in blue, axon in yellow, dendrites absent) and postsynaptic granular cell (green). The top right shows the location of the eight contact sites between the GABAergic axon (yellow) and the axon initial segment of the postsynaptic granular cell (green). (b) An action potential in AAC (1) elicits a small-amplitude, short-latency unitary IPSP in the postsynaptic granular cell (2) that reverses at around −78 mV (traces 2 show averaged EPSPs).
Adapted from Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature368, 823–828, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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14. Figure 19.13 GABAA and GABAB receptor-mediated IPSPs in pyramidal cells.
(a) CA3 pyramidal cells respond to a hilar stimulation by a biphasic IPSP preceded by an EPSP (inset). The biphasic IPSP consist of an early (A) and a late (B) IPSP. (b) In the presence of QX 314 (50 m M) in the pipette solution, stimulation no longer evokes the late IPSP whereas the early one (A) is spared (as well as the EPSP, not shown). The pipette is filled with potassium methyl sulfate (KMeSO4).
Adapted from McLean HA, Ben Ari Y, Gaiarsa JL (1995) NMDA-dependent GABAA-mediated polysynaptic potentials in the neonatal rat hippocampal CA3 region. Eur. J. Neurosci. 7, 1442–1448, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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15. Figure 19.14 Unitary EPSP evoked in an inhibitory interneuron in response to a CA3 pyramidal cell.
(a) A single spike in the presynaptic pyramidal cell (1) evokes a unitary EPSP in the postsynaptic interneuron (2) that fluctuates in amplitude and sometimes fails. An averaged EPSP and an averaged trace of failures (n = 38) are shown below. Av: average. (b) EPSPs initiated in an inhibitory interneuron in response to a single spike (left) or a train of three spikes (right) in the presynaptic pyramidal cell (1). On the right there is a temporal summation of the EPSPs.
Adapted from Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea pig in vitro. J. Physiol. 428, 61–77, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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16. Figure Spike to spike transmission at an excitatory synapse between a CA3 pyramidal neuron and a postsynaptic inhibitory interneuron.
In response to successive single spikes in a presynaptic pyramidal cell (1, only one spike is displayed), one transmission failure, one unitary EPSP and one unitary EPSP that causes postsynaptic firing are recorded in the postsynaptic interneuron (2, three superimposed traces).
Adapted from Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea pig in vitro. J. Physiol. 428, 61–77, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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17. 17 From Cellular and Molecular Neurophysiology, Fourth Edition.
Figure Feedforward inhibition between two CA3 pyramidal cells.
(a) In response to a single spike in one pyramidal cell (1), an IPSP is recorded in a neighboring pyramidal cell (3). Upper trace 2 shows three superimposed responses to three presynaptic action potentials (trace 1, only one spike is displayed). There is one transmission failure and two IPSPs. Middle trace 3 shows the effect of CNQX in the bath: the evoked IPSPs are suppressed but spontaneous ones are still present (arrow). Bottom trace 3 shows the return to control solution. (b) Sequential recordings of the three connected cells. Pyramidal cell 1 activates interneuron 2 (average of uEPSP, n = 40) and interneuron 2 inhibits cell 3 (average of uIPSP, n = 40).
Adapted from Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea pig in vitro. J. Physiol. 428, 61–77, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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18. Figure 19.17 Unitary EPSP evoked in a CA3 pyramidal cell in response to a CA3 pyramidal cell.
(a) Monosynaptic unitary EPSP evoked in a postsynaptic pyramidal cell (2) in response to a single spike in the presynaptic pyramidal cell (1). The EPSP fluctuates in amplitude and sometimes fails. Bottom trace shows an averaged (Av) EPSP. (b) EPSPs initiated in a postsynaptic pyramidal cell (2) in response to a single spike (left) or a train of three spikes (right) in the presynaptic pyramidal cell (1). On the right there is a temporal summation of the EPSPs.
Part (a) adapted from Miles R, Wong RKS (1986) Excitatory synaptic interactions between CA3 neurones in the guinea pig hippocampus. J. Physiol. 373, 397–418, with permission. Part (b) adapted from Miles R (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea pig in vitro. J. Physiol. 428, 61–77, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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19. 19 From Cellular and Molecular Neurophysiology, Fourth Edition.
Figure Sharp waves (SPW) in CA1 of the awake immobile rat and the high-frequency oscillations (ripples).
(a) The extracellular activity of a population of neurons is recorded with nine extracellular electrodes in the CA1 region. (b) Extracellular recordings show that the sharp waves are the most pronounced in the apical dendritic layer (stratum radiatum, RAD). (c) When the recordings in (b) are filtered in order to leave only the events with a frequency between 50 and 250 Hz, high-frequency oscillations that form a ripple are revealed. Ripples are particularly prominent in the pyramidal layer (p). Note that the amplitude scale is increased 5-fold between (b) and (c).
Adapted from Ylinen A, Bragin A, Nadasdy Z et al. (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30–46, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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20. Figure Intracellular activity of a pyramidal neuron and an interneuron during high-frequency oscillations (ripples)
Intracellular recording (a) from a CA1 pyramidal neuron and (b) from a CA1 basket cell (BC) during a single ripple event. In (a), membrane hyperpolarization of the pyramidal cell from −65 to −100 mV reveals a strong depolarization force during the ripple. In (b) arrows indicate spike failures.
Part (a) adapted from Ylinen A, Bragin A, Nadasdy Z et al. (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30–46, with permission. Part (b) adapted from Freund TF, Buzsaki G (1996) Interneurons in the hippocampus. Hippocampus6, 347–470, with permission.
From Cellular and Molecular Neurophysiology, Fourth Edition.
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