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Dissection of cortical microcircuits by single-neuron stimulation in vivo.

ABSTRACT: A fundamental process underlying all brain functions is the propagation of spiking activity in networks of excitatory and inhibitory neurons. In the neocortex, although functional connections between pairs of neurons have been studied extensively in brain slices, they remain poorly characterized in vivo, where the high background activity, global brain states, and neuromodulation can powerfully influence synaptic transmission. To understand how spikes are transmitted in cortical circuits in vivo, we used two-photon calcium imaging to monitor ensemble activity and targeted patching to stimulate a single neuron in mouse visual cortex.Burst spiking of a single pyramidal neuron can drive spiking activity in both excitatory and inhibitory neurons within a ?100 ?m radius. For inhibitory neurons, ?30% of the somatostatin interneurons fire reliably in response to a presynaptic burst of ?5 spikes. In contrast, parvalbumin interneurons showed no detectable responses to single-neuron stimulation, but their spiking is highly correlated with the local network activity.Our results demonstrate the feasibility of mapping functional connectivity at cellular resolution in vivo and reveal distinct operations of two major inhibitory circuits, one detecting single-neuron spike bursts and the other reflecting distributed network activity.

SUBMITTER: Kwan AC

PROVIDER: S-EPMC3467311 | biostudies-literature | 2012 Aug

REPOSITORIES: biostudies-literature

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Dissection of cortical microcircuits by single-neuron stimulation in vivo.

Kwan Alex C AC Dan Yang Y

Current biology : CB 20120628 16

<h4>Background</h4>A fundamental process underlying all brain functions is the propagation of spiking activity in networks of excitatory and inhibitory neurons. In the neocortex, although functional connections between pairs of neurons have been studied extensively in brain slices, they remain poorly characterized in vivo, where the high background activity, global brain states, and neuromodulation can powerfully influence synaptic transmission. To understand how spikes are transmitted in cortic ...[more]

PMID: 22748320

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Project description:The Working Memory model of human memory, first introduced by Baddeley and Hitch (1974), has been one of the most influential psychological constructs in cognitive psychology and human neuroscience. However the neuronal correlates of core components of this model have yet to be fully elucidated. Here we present data from two studies where human temporal cortical single neuron activity was recorded during tasks differentially affecting the maintenance component of verbal working memory. In Study One we vary the presence or absence of distracting items for the entire period of memory storage. In Study Two we vary the duration of storage so that distractors filled all, or only one-third of the time the memory was stored. Extracellular single neuron recordings were obtained from 36 subjects undergoing awake temporal lobe resections for epilepsy, 25 in Study one, 11 in Study two. Recordings were obtained from a total of 166 lateral temporal cortex neurons during performance of one of these two tasks, 86 study one, 80 study two. Significant changes in activity with distractor manipulation were present in 74 of these neurons (45%), 38 Study one, 36 Study two. In 48 (65%) of those there was increased activity during the period when distracting items were absent, 26 Study One, 22 Study Two. The magnitude of this increase was greater for Study One, 47.6%, than Study Two, 8.1%, paralleling the reduction in memory errors in the absence of distracters, for Study One of 70.3%, Study Two 26.3% These findings establish that human lateral temporal cortex is part of the neural system for working memory, with activity during maintenance of that memory that parallels performance, suggesting it represents active rehearsal. In 31 of these neurons (65%) this activity was an extension of that during working memory encoding that differed significantly from the neural processes recorded during overt and silent language tasks without a recent memory component, 17 Study one, 14 Study two. Contrary to the Baddeley model, that activity during verbal working memory maintenance often represented activity specific to working memory rather than speech or language.

Project description:GABA (gamma-aminobutyric acid) is predominantly released by local interneurons in the cerebral cortex to particular subcellular domains of the target cells. This suggests that compartmentalized, synapse-specific action of GABA is required in cortical networks for phasic inhibition. However, GABA released at the synaptic cleft diffuses to receptors outside the postsynaptic density and thus tonically activates extrasynaptic GABA(A) and GABA(B) receptors, which include subtypes of both receptor families especially sensitive to low concentrations of GABA. The synaptic and extrasynaptic action of GABA corroborates the idea that neurons of the brain use synaptic (or wiring) transmission and non-synaptic (or volume) transmission for communication. However, re-uptake mechanisms restrict the spatial extent of extrasynaptic GABA-mediated effects, and it has been proposed that the concerted action of several presynaptic interneurons, the sustained firing of individual cells or an increase in release-site density is required to reach ambient GABA levels sufficient to activate extrasynaptic receptors. Here we show that individual neurogliaform cells release enough GABA for volume transmission within the axonal cloud and, thus, that neurogliaform cells do not require synapses to produce inhibitory responses in the overwhelming majority of nearby neurons. Neurogliaform cells suppress connections between other neurons acting on presynaptic terminals that do not receive synapses at all in the cerebral cortex. They also reach extrasynaptic, delta-subunit-containing GABA(A) (GABA(Adelta)) receptors responsible for tonic inhibition. We show that GABA(Adelta) receptors are localized to neurogliaform cells preferentially among cortical interneurons. Neurosteroids, which are modulators of GABA(Adelta) receptors, alter unitary GABA-mediated effects between neurogliaform cells. In contrast to the specifically placed synapses formed by other interneurons, the output of neurosteroid-sensitive neurogliaform cells represents the ultimate form of the lack of spatial specificity in GABA-mediated systems, leading to long-lasting network hyperpolarization combined with widespread suppression of communication in the local circuit.

Project description:BackgroundThe mirror neuron system (MNS) plays a key role in the neural mechanism underlying motor learning and neural plasticity. Action observation (AO), action execution (AE), and a combination of both, known as action imitation (AI), are the most commonly used rehabilitation strategies based on MNS. It is possible to enhance the cortical activation area and amplitude by combining traditional neuromuscular electrical stimulation (NMES) with other top-down and active rehabilitation strategies based on the MNS theory.ObjectiveThis study aimed to explore the cortical activation patterns induced by NMES synchronized with rehabilitation strategies based on MNS, namely NMES+AO, NMES+AE, and NMES+AI. In addition, the study aimed to assess the feasibility of these three novel rehabilitative treatments in order to provide insights and evidence for the design, implementation, and application of brain-computer interfaces.MethodsA total of 70 healthy adults were recruited from July 2022 to February 2023, and 66 of them were finally included in the analysis. The cortical activation patterns during NMES+AO, NMES+AE, and NMES+AI were detected using the functional Near-Infrared Spectroscopy (fNIRS) technique. The action to be observed, executed, or imitated was right wrist and hand extension, and two square-shaped NMES electrodes were placed on the right extensor digitorum communis. A block design was adopted to evaluate the activation intensity of the left MNS brain regions.ResultsGeneral linear model results showed that compared with the control condition, the number of channels significantly activated (PFDR < 0.05) in the NMES+AO, NMES+AE, and NMES+AI conditions were 3, 9, and 9, respectively. Region of interest (ROI) analysis showed that 2 ROIs were significantly activated (PFDR < 0.05) in the NMES+AO condition, including BA6 and BA44; 5 ROIs were significantly activated in the NMES+AE condition, including BA6, BA40, BA44, BA45, and BA46; and 6 ROIs were significantly activated in the NMES+AI condition, including BA6, BA7, BA40, BA44, BA45, and BA46.ConclusionThe MNS was activated during neuromuscular electrical stimulation combined with an AO, AE, and AI intervention. The synchronous application of NMES and mirror neuron rehabilitation strategies is feasible in clinical rehabilitation. The fNIRS signal patterns observed in this study could be used to develop brain-computer interface and neurofeedback therapy rehabilitation devices.

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Dissection of cortical microcircuits by single-neuron stimulation in vivo.

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Dissection of cortical microcircuits by single-neuron stimulation in vivo.

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