Phase Precession in Hippocampal Interneurons Showing Strong Functional Coupling to Individual Pyramidal Cells

Maurer, Andrew P.; Cowen, Stephen L.; Burke, Sara N.; Barnes, Carol A.; McNaughton, Bruce L.

doi:10.1523/jneurosci.2882-06.2006

Cited by 132 publications

(154 citation statements)

References 35 publications

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“…However, in agreement with previous observations, several interneurons showed definable place fields, although these were typically multiple and less pronounced than those of the pyramidal cells (22,23,25,59). Because spiketransmission probability between place cells and interneurons can be quite reliable (23,26,27), it is expected that some spikes emitted by interneurons are driven by their presynaptic place cells (59). In support of this hypothesis, we found that 8 of the 25 interneurons showed phase precession in at least one location of the track (Fig.…”

Section: Oscillation Frequency Of Place Cells Correlates With Runningsupporting

confidence: 92%

“…59) is the firing-frequency tunability of the pyramidal cell-interneuron synapse (23,(46)(47)(48) and their low-discharge threshold (26,27). Furthermore, soma targeting interneurons are endowed with resonant properties that allow them to respond maximally when presynaptic neurons fire in the ␥-frequency range (23,34), whereas dendrite-targeting interneurons respond best at frequency (49,50).…”

Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

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Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

253

321

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The phase of spikes of hippocampal pyramidal cells relative to the local field oscillation shifts forward (''phase precession'') over a full cycle as the animal crosses the cell's receptive field (''place field''). The linear relationship between the phase of the spikes and the travel distance within the place field is independent of the animal's running speed. This invariance of the phase-distance relationship is likely to be important for coordinated activity of hippocampal cells and space coding, yet the mechanism responsible for it is not known. Here we show that at faster running speeds place cells are active for fewer cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster, yet spatial-phase precession stays unchanged. Interneurons can also show transient-phase precession and contribute to the formation of coherently precessing assemblies. We hypothesize that the speed-correlated acceleration of place cell assembly oscillation is responsible for the phase-distance invariance of hippocampal place cells.cell assembly ͉ interneurons ͉ phase locking ͉ phase precession ͉ oscillations W hile animals navigate in an environment, the hippocampal local field potential (LFP) is characterized by a highly regular oscillation (8-10 Hz). Principal cells in the hippocampus show place-specific firing by two criteria. First, the firing is tuned to a particular location (''place field''), showing a bellshaped tuning curve centered around its preferred location (1). Second, the timing of spikes within subsequent cycles systematically shifts forward (''phase precession''), Ϸ1 full cycle in total, as the rat runs through the place field of the neuron (2, 3) (see also Fig. 1 A and B). Both the firing rate and discharge phase within a cycle are correlated with the rat's position. However, how the rate change and -phase precession of spikes are related is poorly understood. The available experiments support both a rate-phase interdependence (4-6) and independence (7).Several explanations for the place-phase relationship were put forward (4)(5)(6)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). To confront these models, we examined the relationship among running speed, oscillation frequency of place cells and LFP , and timing of spikes within the cycle. We show that principal cells oscillate at a frequency faster than the simultaneously recorded LFP oscillation, and that this oscillation frequency depends on the rat's running speed. Together with the place-and speed-dependent oscillation frequencies of interneurons, the findings support the hypothesis that place coding results from coordinated network activity. We propose that the locomotion speed-dependent oscillation of place cell assemblies may underlie the mechanisms responsible for distance encoding in the hippocampus. ResultsWe recorded the firing patterns of pyramidal cells, interneurons, and the LFP from the CA1 pyramidal layer of rats as they ran on a U-shap...

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Section: Oscillation Frequency Of Place Cells Correlates With Runningsupporting

confidence: 92%

Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

253

321

View full text Add to dashboard Cite

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“…However, research on interneurons in drug-free animals that can freely change their behavior, has so far been limited to recordings from unidentified interneurons because of technical limitations. In the barrel cortex of head-restrained mice, groups of interneurons with distinct membrane dynamics during different behavioral states have been described 16,17 and in the hippocampus unidentified interneurons or interneurons belonging to heterogeneous groups expressing parvalbumin and/or somatostatin have been reported [18][19][20][21] to fire with different firing patterns during network oscillations. But, how do specific types of identified interneurons control the activity of cortical circuits in freely-moving animals?…”

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confidence: 99%

Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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A large variety of GABAergic interneurons control information processing in hippocampal circuits governing the formation of neuronal representations. Whether distinct hippocampal interneuron types contribute differentially to information-processing during behavior is not known. We employed a novel technique for recording and labeling interneurons and pyramidal cells in drug-free, freely-moving rats. Recorded parvalbumin-expressing basket interneurons innervate somata and proximal pyramidal cell dendrites, whereas nitric-oxide-synthase-and neuropeptide-Y-expressing ivy cells provide synaptic and extrasynaptic dendritic modulation. Basket and ivy cells showed distinct spike timing dynamics, firing at different rates and times during theta and ripple oscillations. Basket but not ivy cells changed their firing rates during movement, sleep and quiet wakefulness, suggesting that basket cells coordinate cell assemblies in a behavioral state-contingent manner, whereas persistently-firing ivy cells might control network excitability and homeostasis. Different interneuron types provide GABA to specific subcellular domains at defined times and rates, thus differentially controlling network activity during behavior.GABAergic interneurons control information processing in cortical circuits as percussionists set the rhythm for a melody, or traffic lights regulate the movement of cars through a city. Interneurons generate oscillatory activity 1, 2 , synchronize the activity of pyramidal cells 3 and set time windows for synaptic integration 4 . A large diversity of interneuronal types is a hallmark of cortical circuits. Different domains of pyramidal cells, such as the soma, axoninitial-segment, proximal or distal dendrites 5 are innervated by distinct types of GABAergic interneuron. They also have distinct inputs and membrane properties 6-10 and show different firing patterns during network oscillations induced in vitro [11][12][13][14] or recorded in anesthetized animals 15 , indicating distinct roles for specific interneuron types. However, research on interneurons in drug-free animals that can freely change their behavior, has so far been limited to recordings from unidentified interneurons because of technical limitations. In the barrel cortex of head-restrained mice, groups of interneurons with distinct membrane dynamics during different behavioral states have been described 16,17 and in the hippocampus unidentified interneurons or interneurons belonging to heterogeneous groups expressing parvalbumin and/or somatostatin have been reported [18][19][20][21] to fire with different firing patterns during network oscillations. But, how do specific types of identified interneurons control the activity of cortical circuits in freely-moving animals? CouldCorrespondence and requests for materials should be addressed to D.L. (damien.lapray@pharm.ox.ac.uk) Results Identification of neurons recorded in freely-moving ratsWe recorded the activity of parvalbumin (PV)-expressing basket, ivy and pyramidal cells in the dorsal CA...

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“…subsequent papers has confirmed and refined this observation (e.g., Skaggs et al, 1996;Yamaguchi, Aota, McNaughton, & Lipa, 2002;Harris et al, 2002;Mehta et al, 2002;Huxter, Burgess, & O'Keefe, 2003;Dragoi & Buzsáki, 2006;Maurer, Cowen, Burke, Barnes, & McNaughton, 2006a;Chen & Frank, 2007; see also the reviews by McNaughton, 2007, andYamaguchi et al, 2007). Phase precession exists in both CA3 and CA1 pyramidal cells, but it is much less pronounced in CA1 interneurons (Maurer, Cowen, Burke, Barnes, & McNaughton, 2006b;Ego-Stengel & Wilson, 2007) and the dentate gyrus Yamaguchi et al, 2002). Recently phase precession has been reported in layer II of the medial entorhinal cortex (Fyhn, Hafting, Moser, & Moser, 2006), which provides input to the hippocampus.…”

Section: Introductionmentioning

confidence: 88%

“…Phase precession has mainly been described in CA3 and CA1 pyramidal cells, but it is less pronounced in CA1 interneurons (Maurer et al, 2006b;Ego-Stengel & Wilson, 2007) and the dentate gyrus Yamaguchi et al, 2002). In both latter cases, phase precession might be inherited from CA pyramidal neurons: for CA1 interneurons directly from CA1 pyramidal cells and for cells in the DG by feedback from CA3 via mossy cells.…”

Section: Phase Precession In the Hippocampal Formation And The Entorhmentioning

confidence: 99%

Phase Precession Through Synaptic Facilitation

et al. 2008

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Phase precession is a relational code that is thought to be important for episodic-like memory, for instance, the learning of a sequence of places. In the hippocampus, places are encoded through bursting activity of socalled place cells. The spikes in such a burst exhibit a precession of their firing phases relative to field potential theta oscillations (4-12 Hz); the theta phase of action potentials in successive theta cycles progressively decreases toward earlier phases. The mechanisms underlying the generation of phase precession are, however, unknown. In this letter, we show * Kay Thurley is now at the Institute of Physiology, University of Bern, 3012 Bern, Switzerland. Christian Leibold is now at the Department of Biology II, LudwigMaximilians-Universität München, 82152 Planegg-Martinsried, Germany. through mathematical analysis and numerical simulations that synaptic facilitation in combination with membrane potential oscillations of a neuron gives rise to phase precession. This biologically plausible model reproduces experimentally observed features of phase precession, such as (1) the progressive decrease of spike phases, (2) the nonlinear and often also bimodal relation between spike phases and the animal's place, (3) the range of phase precession being smaller than one theta cycle, and (4) the dependence of phase jitter on the animal's location within the place field. The model suggests that the peculiar features of the hippocampal mossy fiber synapse, such as its large efficacy, long-lasting and strong facilitation, and its phase-locked activation, are essential for phase precession in the CA3 region of the hippocampus. Neural Computation

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Phase Precession in Hippocampal Interneurons Showing Strong Functional Coupling to Individual Pyramidal Cells

Cited by 132 publications

References 35 publications

Hippocampal place cell assemblies are speed-controlled oscillators

Hippocampal place cell assemblies are speed-controlled oscillators

Behavior-dependent specialization of identified hippocampal interneurons

Phase Precession Through Synaptic Facilitation

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