Whole-Cell Recordings in Freely Moving Rats

Lee, Albert K.; Manns, Ian D.; Sakmann, Bert; Brecht, Michael

doi:10.1016/j.neuron.2006.07.004

Cited by 245 publications

(182 citation statements)

References 33 publications

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“…The evaluation of rate-specific synchrony in vivo would be best performed by dual intracellular recording in awake animals, which, despite experimental advances (24,25), remains technically challenging. However, a signature of rate-specific synchrony in extracellular recordings would be cross-correlation histograms that exhibit high peak amplitudes when rates are similar and gamma oscillations are present.…”

Section: Discussionmentioning

confidence: 99%

Rate-specific synchrony: Using noisy oscillations to detect equally active neurons

Markowitz¹,

Collman²,

Brody

et al. 2008

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

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Although gamma frequency oscillations are common in the brain, their functional contributions to neural computation are not understood. Here we report in vitro electrophysiological recordings to evaluate how noisy gamma frequency oscillatory input interacts with the overall activation level of a neuron to determine the precise timing of its action potentials. The experiments were designed to evaluate spike synchrony in a neural circuit architecture in which a population of neurons receives a common noisy gamma oscillatory synaptic drive while the firing rate of each individual neuron is determined by a slowly varying independent input. We demonstrate that similarity of firing rate is a major determinant of synchrony under common noisy oscillatory input: Near coincidence of spikes at similar rates gives way to substantial desynchronization at larger firing rate differences. Analysis of this rate-specific synchrony phenomenon reveals distinct spike timing ''fingerprints'' at different firing rates that emerge through a combination of phase shifting and abrupt changes in spike patterns. We further demonstrate that rate-specific synchrony permits robust detection of rate similarity in a population of neurons through synchronous activation of a postsynaptic neuron, supporting the biological plausibility of a Many Are Equal computation. Our results reveal that spatially coherent noisy oscillations, which are common throughout the brain, can generate previously unknown relationships among neural rate codes, noisy interspike intervals, and precise spike synchrony codes. All of these can coexist in a self-consistent manner because of rate-specific synchrony.gamma oscillations ͉ neural code ͉ neural computation G amma oscillations (30-100 Hz) are observed in field potential recordings from many brain areas (1-4). These oscillations are typically noisy, exhibiting fluctuations in amplitude and a broad frequency distribution. In vitro experiments using cortical brain slices (5) have demonstrated that gamma oscillations can be produced by sustained activation of networks of inhibitory neurons, which in turn produce highly correlated rhythmic membrane potential oscillations in the local population of pyramidal cells (6). This raises the general question of what role common noisy oscillatory synaptic inputs might play in producing synchronous action potentials across a population of neurons with differing mean firing rates. In the presence of correlated noisy gamma, neurons with the same mean firing rate would be expected to produce highly correlated spike trains (7). But what is the level of synchrony that will result when the mean firing rates are different? These correlations would be functionally important because relative spike timing on the millisecond time scale influences synaptic activation of postsynaptic targets (8, 9), timing-dependent short-term synaptic plasticity (10, 11), and pattern recognition (12).Previous work has shown that weakly correlated noisy input to a pair of neurons produces an output correlation p...

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Section: Discussionmentioning

confidence: 99%

Rate-specific synchrony: Using noisy oscillations to detect equally active neurons

Markowitz¹,

Collman²,

Brody

et al. 2008

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

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“…A glass electrode, containing 1.5 or 3 % neurobiotin in 0.5 M NaCl, mounted on a custom-made hydraulic (Narishige) or piezoelectric 45 (Kleindiek Nanotechnik) microdrive, was inserted into the cortex. A miniature pre-amplifier (ELC mini-preamplifier, NPI Electronic) and two 46 , but recording from hippocampal neurons started more than one hour after recovery from anesthesia (109.4 ± 55.1 min; only two pyramidal cells were recorded before one hour, after 25 and 50 min respectively, neither was labeled).…”

Section: Juxtacellular Recording and Labeling In Freely Moving Ratsmentioning

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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“…Although one major limitation of conventional MP imaging has been the need to firmly hold the skull in position to prevent the brain from moving relative to the microscope objective, some aspects of free movement can be simulated in head-fixed animals by placing them in a virtual reality situation (11). For measurements in truly free-moving animals, the recording apparatus must be miniaturized and attached to the skull, similar to the approach used for the recording of extracellular (1,12) and intracellular (13) electrical signals in freely moving rodents. It is possible to use optical fibers to deliver short-pulse light suitable for two-photon excitation, scan the excitation focus, and collect the emitted fluorescence (14).…”

mentioning

confidence: 99%

Visually evoked activity in cortical cells imaged in freely moving animals

Sawiński

Wallace

Greenberg

et al. 2009

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

207

172

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We describe a miniaturized head-mounted multiphoton microscope and its use for recording Ca 2؉ transients from the somata of layer 2/3 neurons in the visual cortex of awake, freely moving rats. Images contained up to 20 neurons and were stable enough to record continuously for >5 min per trial and 20 trials per imaging session, even as the animal was running at velocities of up to 0.6 m/s. Neuronal Ca 2؉ transients were readily detected, and responses to various static visual stimuli were observed during free movement on a running track. Neuronal activity was sparse and increased when the animal swept its gaze across a visual stimulus. Neurons showing preferential activation by specific stimuli were observed in freely moving animals. These results demonstrate that the multiphoton fiberscope is suitable for functional imaging in awake and freely moving animals.calcium imaging ͉ head-mounted microscope ͉ neuronal activity ͉ two-photon ͉ visual cortex T he observation of neural activity has been central to the vast majority of efforts to understand information processing in the mammalian brain. Although some aspects of sensory processing can be studied in animals that are anesthetized or awake but head-fixed, to fully understand awake information processing, animals must be able to interact fully with their environment. Previously, this approach, which includes both allothetic and idiothetic cues, lead to the discovery of place cells (1), head-direction cells (2), and grid cells (3). Multiphoton (MP) imaging (4) of neurons bulk-loaded with calcium indicators (5-7) allows not only the unambiguous identification and precise anatomical localization of active neurons but also the simultaneous recording of activity in multiple neurons even at very low firing rates (8-10). Although one major limitation of conventional MP imaging has been the need to firmly hold the skull in position to prevent the brain from moving relative to the microscope objective, some aspects of free movement can be simulated in head-fixed animals by placing them in a virtual reality situation (11). For measurements in truly free-moving animals, the recording apparatus must be miniaturized and attached to the skull, similar to the approach used for the recording of extracellular (1, 12) and intracellular (13) electrical signals in freely moving rodents. It is possible to use optical fibers to deliver short-pulse light suitable for two-photon excitation, scan the excitation focus, and collect the emitted fluorescence (14). There have been a number of recent advances in scanning technology (15, 16) that have been applied to anesthetized animals by using two-photon excitation (17) or freely moving animals by using one-photon wide-field imaging (18). Here we show that it is possible to use two-photon microscopy to record activity from neuronal populations with cellular resolution in freely moving animals. Results and DiscussionWe developed a fiberscope (Fig. 1 A) that employs a customdesigned water-immersion lens and a leveraged, nonresonant fiber scan...

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Whole-Cell Recordings in Freely Moving Rats

Cited by 245 publications

References 33 publications

Rate-specific synchrony: Using noisy oscillations to detect equally active neurons

Rate-specific synchrony: Using noisy oscillations to detect equally active neurons

Behavior-dependent specialization of identified hippocampal interneurons

Visually evoked activity in cortical cells imaged in freely moving animals

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