Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents

Pike, Fenella G.; Goddard, Ruth S.; Suckling, Jillian M.; Ganter, Paul; Kasthuri, Narayanan; Paulsen, Ole

doi:10.1111/j.1469-7793.2000.00205.x

Cited by 340 publications

(350 citation statements)

References 31 publications

(48 reference statements)

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“…One possible explanation for the speed effect on the oscillation frequency of place cells is that the frequency is controlled by the activation of voltage-dependent intrinsic mechanisms that support oscillations in single pyramidal cells (5,8,9,13,(30)(31)(32)(33)(34). However, this individuated oscillation cannot account for several experimental observations (7,24,35).…”

Section: Speed-dependent Oscillation Of Place Cells Can Keep the Spikmentioning

confidence: 79%

“…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). Therefore, the recruited interneurons have the ability to segregate small assemblies of principal cells by temporarily silencing competing assemblies.…”

Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

See 1 more Smart Citation

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

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

249

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: Speed-dependent Oscillation Of Place Cells Can Keep the Spikmentioning

confidence: 79%

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.

249

321

View full text Add to dashboard Cite

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“…When the stimulus amplitude is increased above the spike threshold, the firing rate, reliability and precision will be optimal for stimulus waveforms at the neuron's preferred frequency. Experiments show that preferred frequencies depend on neuron types 23,30,31 . Models predict that the preferred frequency arises from the dynamics of voltage-gated channels [32][33][34] .…”

Section: Stimulus Locking and Phase Lockingmentioning

confidence: 99%

Regulation of spike timing in visual cortical circuits

2008

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A train of action potentials (a spike train) can carry information in both the average firing rate and the pattern of spikes in the train. But can such a spike-pattern code be supported by cortical circuits? Neurons in vitro produce a spike pattern in response to the injection of a fluctuating current. However, cortical neurons in vivo are modulated by local oscillatory neuronal activity and by top-down inputs. In a cortical circuit, precise spike patterns thus reflect the interaction between internally generated activity and sensory information encoded by input spike trains. We review the evidence for precise and reliable spike timing in the cortex and discuss its computational role.Reliability and precision are two different quantities. When you make an appointment with your friend, she can either keep the appointment or not show up at all. If she does show up, she might or might not be on time. The former uncertainty is related to reliability, whereas the latter is related to precision. When the same stimulus waveform is repeatedly injected at the soma of a neuron in vitro (FIG. 1a), a similar spike train is obtained on each trial 1,2 (FIG. 1b). When approximately the same number of spikes occur on each trial the neuron is said to be reliable, whereas when the spikes occur almost at the same time across trials it is said to be precise (FIG. 1c). For a single neuron, the potential information content of precise and reliable spike times is many times larger than that which is contained in the firing rate, which is averaged across a typical interval of a hundred milliseconds [3][4][5][6] . The information contained in spike timing is available immediately, rather than after an averaging period. Furthermore, the timing of patterns of spikes can potentially transmit even more information than the timing of the individual constituent spikes 3,7 . The potential relevance of spike patterns becomes apparent when we consider neurons at the population level: when a group of similar neurons (a 'pool') produces precise and reliable spike trains, the neurons they project to receive volleys of synchronous spikes 8,9 . This opens up the possibility of communicating between different cortical areas through synchronous spike volleys.In contrast to the in vitro situation described above, in the intact cortex most excitatory synaptic inputs arrive at the dendrites rather than at the soma (FIG. 1d), and synaptic transmission is typically unreliable [10][11][12][13] . Furthermore, most of these dendritic inputs are not directly related to ongoing sensory stimulation; rather, they reflect spatiotemporally structured internal activity. Therefore, when the same stimulus is presented repeatedly, the resulting spike trains are usually neither precise nor reliable when they are aligned to the stimulus onset 6 . Instead, HHMI Author ManuscriptHHMI Author Manuscript HHMI Author Manuscript neural activity in vivo might be dominated by internally generated complex reverberations or rhythmic oscillations, and precise and reliable sp...

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“…Because membrane-intrinsic oscillatory properties (24) of O-LM cells are an important determinant of their discharge pattern, we tested whether these properties changed. Interneurons, depolarized near spike threshold by positive current injection (usually Ͻ50 pA), showed a MP oscillation in the theta band in both control and epileptic slices.…”

Section: O-lm Interneuron-discharge Frequency Shifts From the Theta Tmentioning

confidence: 99%

Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy

Dugladze

Vida

Tort

et al. 2007

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

121

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Mesial temporal lobe epilepsy (mTLE) is one of the most common forms of epilepsy, characterized by hippocampal sclerosis and memory deficits. Injection of kainic acid (KA) into the dorsal hippocampus of mice reproduces major electrophysiological and histopathological characteristics of mTLE. In extracellular recordings from the morphologically intact ventral hippocampus of KA-injected epileptic mice, we found that theta-frequency oscillations were abolished, whereas gamma oscillations persisted both in vivo and in vitro. Whole-cell recordings further showed that oriens-lacunosum-moleculare (O-LM) interneurons, key players in the generation of theta rhythm, displayed marked changes in their intrinsic and synaptic properties. Hyperpolarization-activated mixed cation currents (Ih) were significantly reduced, resulting in an increase in the input resistance and a hyperpolarizing shift in the resting membrane potential. Additionally, the frequency of spontaneous excitatory postsynaptic currents (sEPSCs) was increased, indicating a stronger excitatory input to these neurons. As a consequence, O-LM interneurons increased their firing rate from theta to gamma frequencies during induced network activity in acute slices from KA-injected mice. Thus, our physiological data together with network simulations suggest that changes in excitatory input and synaptic integration in O-LM interneurons lead to impaired rhythmogenesis in the hippocampus that in turn may underlie memory deficit.in vitro ͉ interneurons ͉ oscillations ͉ patch-clamp ͉ in vivo

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Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents

Cited by 340 publications

References 31 publications

Hippocampal place cell assemblies are speed-controlled oscillators

Hippocampal place cell assemblies are speed-controlled oscillators

Regulation of spike timing in visual cortical circuits

Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy

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