EEG alpha oscillations: The inhibition–timing hypothesis

GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits

Genetic methods available in mice are likely to be powerful tools in dissecting cortical circuits. However, the visual cortex, in which sensory coding has been most thoroughly studied in other species, has essentially been neglected in mice perhaps because of their poor spatial acuity and the lack of columnar organization such as orientation maps. We have now applied quantitative methods to characterize visual receptive fields in mouse primary visual cortex V1 by making extracellular recordings with silicon electrode arrays in anesthetized mice. We used current source density analysis to determine laminar location and spike waveforms to discriminate putative excitatory and inhibitory units. We find that, although the spatial scale of mouse receptive fields is up to one or two orders of magnitude larger, neurons show selectivity for stimulus parameters such as orientation and spatial frequency that is near to that found in other species. Furthermore, typical response properties such as linear versus nonlinear spatial summation (i.e., simple and complex cells) and contrast-invariant tuning are also present in mouse V1 and correlate with laminar position and cell type. Interestingly, we find that putative inhibitory neurons generally have less selective, and nonlinear, responses. This quantitative description of receptive field properties should facilitate the use of mouse visual cortex as a system to address longstanding questions of visual neuroscience and cortical processing.

https://www.jneurosci.org/content/jneuro/28/30/7520.full.pdf

Highly Selective Receptive Fields in Mouse Visual Cortex

The lateral geniculate nucleus is the best understood thalamic relay and serves as a model for all thalamic relays. Only 5-10% of the input to geniculate relay cells derives from the retina, which is the driving input. The rest is modulatory and derives from local inhibitory inputs, descending inputs from layer 6 of the visual cortex, and ascending inputs from the brainstem. These modulatory inputs control many features of retinogeniculate transmission. One such feature is the response mode, burst or tonic, of relay cells, which relates to the attentional demands at the moment. This response mode depends on membrane potential, which is controlled effectively by the modulator inputs. The lateral geniculate nucleus is a first-order relay, because it relays subcortical (i.e. retinal) information to the cortex for the first time. By contrast, the other main thalamic relay of visual information, the pulvinar region, is largely a higher-order relay, since much of it relays information from layer 5 of one cortical area to another. All thalamic relays receive a layer-6 modulatory input from cortex, but higher-order relays in addition receive a layer-5 driver input. Corticocortical processing may involve these corticothalamocortical 're-entry' routes to a far greater extent than previously appreciated. If so, the thalamus sits at an indispensable position for the modulation of messages involved in corticocortical processing.

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The role of the thalamus in the flow of information to the cortex

Most neuronal interactions in the cortex occur within local circuits. Because principal cells and GABAergic interneurons contribute differently to cortical operations, their experimental identification and separation is of utmost important. We used 64-site two-dimensional silicon probes for high-density recording of local neurons in layer 5 of the somatosensory and prefrontal cortices of the rat. Multiple-site monitoring of units allowed for the determination of their two-dimensional spatial position in the brain. Of the approximately 60,000 cell pairs recorded, 0.2% showed robust short-term interactions. Units with significant, short-latency (<3 ms) peaks following their action potentials in their cross-correlograms were characterized as putative excitatory (pyramidal) cells. Units with significant suppression of spiking of their partners were regarded as putative GABAergic interneurons. A portion of the putative interneurons was reciprocally connected with pyramidal cells. Neurons physiologically identified as inhibitory and excitatory cells were used as templates for classification of all recorded neurons. Of the several parameters tested, the duration of the unfiltered (1 Hz to 5 kHz) spike provided the most reliable clustering of the population. High-density parallel recordings of neuronal activity, determination of their physical location and their classification into pyramidal and interneuron classes provide the necessary tools for local circuit analysis.

http://www.buzsakilab.com/content/PDFs/Bartho2004JNeurophys.pdf

Characterization of Neocortical Principal Cells and Interneurons by Network Interactions and Extracellular Features

Considerable effort has gone into understanding the mechanisms underlying high-frequency 'bursting' of thalamocortical impulses, their sensory information content and their involvement in perception. However, little is known about the influence of such impulses on their cortical targets. Here we follow bursting thalamic impulses to their terminus at the thalamocortical synapse of the awake rabbit, and examine their influence on a class of somatosensory cortical neurons. We show that thalamic bursts potently activate cortical circuits. Initial impulses of each burst have a greatly enhanced ability to elicit cortical action potentials, and later impulses in the burst further raise the probability of eliciting spikes. In some cases, multiple cortical spikes result from a single burst. Moreover, we show that the interval preceding each burst is crucial for generating the enhanced cortical response. The powerful activation of neocortex by thalamocortical bursts is fully consistent with an involvement of these impulses in perceptual/attentional processes.

The impact of 'bursting' thalamic impulses at a neocortical synapse

Thalamocortical (TC) impulses potently influence the sensory neocortex, but the functional impact of individual TC neurons throughout the layers of the cortex has proved difficult to assess. Here we examine, in awake rabbits, the vertical distribution of monosynaptic currents generated in a somatosensory cortical "barrel" column by spontaneous impulses of single, topographically aligned TC neurons. We show that closely neighboring TC neurons generate widely differing patterns of monosynaptic activation within layers 4 and 6 of their aligned column. Moreover, synaptic currents generated by TC impulses with long preceding interspike intervals are greatly enhanced in both of these layers. The degree of this enhancement differs reliably among neighboring TC neurons but, for a given neuron, is very similar in layers 4 and 6. Our results indicate that in the awake state, TC synapses throughout the depth of the cortex serve as powerful filters of sensory information that reflect individual characteristics of their parent TC neuron.

https://www.jneurosci.org/content/jneuro/22/17/7766.full.pdf

Activation of a Cortical Column by a Thalamocortical Impulse

In the somatosensory 'barrel' cortex1 (where each barrel represents an individual whisker) the receptive fields of cortical spiny neurons show considerable specificity for the direction of whisker displacement, as do the receptive fields of thalamocortical (TC) neurons that provide input to the barrels In contrast, putative fast-spike inhibitory interneurons in layer 4 of the barrel cortex lack directional preference, but are exquisitely sensitive to low stimulus intensities2,3 Here we show, in adult rabbits, that these sensitive and broadly tuned inhibitory receptive fields are generated by an unselective pooling of convergent functional inputs from topographically aligned TC neurons with very diverse response properties

Receptive-field construction in cortical inhibitory interneurons.

Extracellular recordings were obtained from single neurons in ventrobasal (VB) thalamus of awake rabbits while field potentials were recorded at various depths within topographically aligned and no...

The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex.

We used spike-triggered current source-density analysis to examine axonal and postsynaptic currents generated in the visual cortex of awake rabbits by spontaneous spikes of individual sustained and transient dorsal lateral geniculate nucleus (LGNd) neurons. Using these data, we asked whether sustained/transient sensory responses are related to short-term synaptic dynamics at the thalamocortical synapse. Most sustained (34 of 40) and transient (24 of 25) neurons generated axonal and monosynaptic responses in layer 4 and/or 6 of the aligned cortical domain, with input from transient neurons arriving ∼0.3 ms earlier and 100–200 μm deeper. Postsynaptic cortical responses generated by both thalamic cell classes were reduced in amplitude after a preceding impulse and slowly recovered over a period of >750 ms. We interpret this to reflect interval-dependent recovery from chronic depression at the thalamocortical synapse, caused by significant spontaneous firing of LGNd cells (∼8 Hz). Surprisingly, postsynaptic cortical responses generated by spontaneous spikes of sustained thalamic neurons were more depressed than those of transient neurons. This difference was seen both in layers 4 and 6. The depression saturated rapidly with multiple preceding impulses, and postsynaptic responses generated by sustained neurons during maintained visual stimulation remained sufficiently robust to allow a sustained flow of information to the cortex. Our results indicate a relationship between the sensory response properties of thalamic neurons and the short-term dynamics of their synapses, and suggest that cortical recipients of sustained and transient thalamic inputs will differ considerably in their response modulation by prior impulse activity.

https://www.jneurosci.org/content/jneuro/28/19/5018.full.pdf

Alexander G. Gusev

Papers

The impact of 'bursting' thalamic impulses at a neocortical synapse

Activation of a Cortical Column by a Thalamocortical Impulse

Receptive-field construction in cortical inhibitory interneurons.

The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex.

The Impact of an LGNd Impulse on the Awake Visual Cortex: Synaptic Dynamics and the Sustained/Transient Distinction