Fast-spike units, feedforward inhibition and thalamocortical response transformations in the somatosensory system.
In the rodent somatosensory cortex, identifiable groups of local circuit neurons, called ‘barrels’, are related one-to-one to individual vibrissae, or whiskers, on the contralateral face. The spatial relationship between whiskers and barrels is elegant and compelling, but perhaps the true elegance of the system lies in its functioning in the temporal domain. Circuit dynamics create a "window of opportunity" for synchronous thalamic inputs to engage momentarily barrel circuitry before local inhibition damps the excitatory response. Critical insights into the nature of circuit operations stem from consistently observed differences in the response properties of thalamocortical units (TCUs), barrel regular-spike units (RSUs; presumed excitatory neurons) and barrel fast-spike units (FSUs; presumed inhibitory neurons). Of the three cell types, FSUs have the highest spontaneous and stimulus-evoked firing rates, they respond more uniformly to different directions of whisker deflection, and they include more whiskers in their receptive fields. FSU receptive field properties thus reflect the combination of their TC inputs. RSUs on average fire more sparsely and are more tuned than TCUs and FSUs; they respond more non-linearly such that their receptive field properties reflect the commonality of their TCU inputs. FSU and RSU properties are consistent with anatomical findings that TC neurons make synapses onto inhibitory neuron cell bodies and proximal dendrites and functional data showing that TCUs make stronger and more convergent connections onto FSUs than RSUs. Moreover, due to intrinsic properties FSUs can fire at higher rates. Highly effective, relatively non-specific afferent activation of FSUs provides strong and rapid feedforward inhibition that works in conjunction with neuronal and network non-linearities to enhance response tuning in barrel RSUs, the major source of afferent excitation to the rest of the cortical column.
