Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex

Abstract

'Fast-spike' interneurons of layer 4 mediate thalamocortical feedforward inhibition and can, with some confidence, be identified using extracellular methods. In somatosensory barrel cortex of awake rabbits, these 'suspected inhibitory interneurons' (SINs) have distinct receptive field properties: they respond to vibrissa displacement with very high sensitivity and temporal fidelity. However, they lack the directional specificity that is clearly seen in most of their ventrobasal thalamocortical afferents. Several lines of evidence show that layer-4 SINs receive a potent and highly convergent and divergent functional input from topographically aligned thalamocortical neurons. Whereas the unselective pooling of convergent thalamocortical inputs onto SINs generates sensitive and broadly tuned inhibitory receptive fields, the potent divergence of single thalamocortical neurons onto many SINs generates sharply synchronous (+/-1 ms) activity (because of coincident EPSPs). Synchronous discharge of these interneurons following thalamocortical impulses will generate a synchronous feedforward release of GABA within the barrel. Thalamocortical impulses will, therefore, generate only a brief 'window of excitability' during which spikes can occur in the post-synaptic targets of fast-spike interneurons. This fast, synchronous, highly sensitive and broadly tuned feed-forward inhibitory network is well suited to suppress spike generation in spiny neurons following all but the most optimal feedforward excitatory inputs.

Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model

“…This does not imply that all such neurons must be nonselective (see refs. [40][41][42][43][44][45]. For instance, the results of ref.…”

Differential Involvement of Excitatory and Inhibitory Neurons of Cat Motor Cortex in Coincident Spike Activity Related to Behavioral Context

“…Neurons in the present study were classified as RS, FS, or "unspecified" based on analysis of their extracellular spiking features, but only RS and FS neurons were included in this analysis. Combined morphological and physiological studies have revealed that in most instances RS and FS neurons may be reliably identified as pyramidal neurons and inhibitory interneurons, respectively (McCormick et al, 1985;Rao et al, 1999;Tanaka, 1999;Compte et al, 2000;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Isomura et al, 2009). "Baseline firing rate" was defined as the average firing rate recorded from a neuron when the animal was sitting quietly.…”

“…Recent studies have distinguished spiny (excitatory) and nonspiny (inhibitory) neurons based on characteristics of extracellular spikes (McCormick et al, 1985;Kawaguchi, 1995;Cauli et al, 1997;Rao et al, 1999;Compte et al, 2000;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Isomura et al, 2009). Studies investigating functional interactions between fast-spiking (FS, interneuron) and regular-spiking (RS, pyramidal) neurons in motor and nonmotor areas of cerebral cortex have shown that the incidence of these interactions can vary between different neuronal subtypes (Rao et al, 1999;Tanaka, 1999;Compte et al, 2000;Constantinidis and Goldman-Rakic, 2002;Swadlow, 2003;Merchant et al, 2008;Isomura et al, 2009). Again, similar studies are yet to be performed during different behaviors.…”

Excitability of cortical neurons depends upon a powerful tonic conductance in inhibitory networks

“…First, FS cells are fast-spiking, which, we speculate might mean that they contribute more to the ambient concentration of GABA than LTS cells. Second, FS cells receive direct thalamocortical input (Gibson et al, 1999;Beierlein et al, 2000;Porter et al, 2001;Swadlow, 2003), which puts them in a more direct position to be regulated by thalamocortical bursting than LTS cells. Finally, FS cells are inhibited, whereas LTS cells are excited, by acetylcholine (Xiang et al, 1998).…”

“…Large bundles of fibers from the bar-reloids in the ventral posterior medial nucleus of the thalamus project to individual barrels in layer 4 (Woolsey and Van der Loos, 1970). These thalamocortical fibers synapse onto excitatory neurons and onto a type of inhibitory interneuron neuron (White and Keller, 1987) called fast-spiking (FS) cells that mediate feed-forward inhibition (Porter et al, 2001;Swadlow, 2003). Thus, inhibition is recruited at a very early stage in sensory processing.…”