Linear transformation of thalamocortical input by intracortical excitation

Abstract

Neurons in thalamorecipient layers of sensory cortices integrate thalamocortical and intracortical inputs. Although their functional properties can be inherited from the convergence of thalamic inputs, the roles of intracortical circuits in thalamocortical transformation of sensory information remain unclear. Here, by reversibly silencing intracortical excitatory circuits with optogenetic activation of parvalbumin-positive inhibitory neurons in mouse primary visual cortex, we compared visually-evoked thalamocortical input with total excitation in the same layer 4 pyramidal neurons. We found that intracortical excitatory circuits preserve the orientation and direction tuning of thalamocortical excitation, with a linear amplification of thalamocortical signals by about threefold. The spatial receptive field of thalamocortical input is slightly elongated, and is expanded by intracortical excitation in an approximately proportional manner. Thus, intracortical excitatory circuits faithfully reinforce the representation of thalamocortical information, and may influence the size of the receptive field by recruiting additional inputs.

Formation and maintenance of neuronal assemblies through synaptic plasticity

“…Our model, however, makes predictions that can be tested with single neurons or pairs (Figs 8 and 9). One prediction, that recurrent connectivity is responsible for a large proportion of stimulus-tuned excitatory input, is consistent with findings from visual and auditory cortex that tuned recurrent excitation amplifies responses to thalamic input [46][47][48] . The fact that these responses are associated with slow dynamics 18 is also consistent with results from auditory cortex, suggesting that recurrent excitation prolongs response duration 48 .…”

Functional organization of excitatory synaptic strength in primary visual cortex

“…4g, h). These results suggest that local connections contribute to the stimulus selectivity of L2/3 neurons by providing tuned excitation that modulates the membrane potential in a manner qualitatively similar to that observed in vivo [19][20][21][22][23] .…”

“…In mouse V1, a simple cell's subthreshold response to drifting grating stimuli [19][20][21][22][23] is characterized by two components that are determined by the angle and phase of the grating in relation to its RF (Fig. 4a).…”

“…This circuit architecture-comprising strong recurrent excitation within ensembles of neurons with similar RFs-may additionally amplify (and perhaps prolong 25 ) populationlevel responses to particular sensory stimuli 19,20,[26][27][28][29] , and thus promote effective information transmission to multiple postsynaptic targets. In contrast, the matrix of more numerous, weaker connections, which only generate a small fraction of total excitation in the L2/3 network, may facilitate local contextual interactions and serve as a substrate for plasticity-for example, when particular visual feature combinations become behaviourally relevant.…”

Functional organization of synaptic connections in the neocortex

“…Therefore, we revealed that the connectivity between L2/3 neurons in V1 is highly specific, though nonexclusive, with respect to their feature selectivity. Such a specific connection scheme may serve to amplify the incoming thalamic signal by providing strong excitation that is closely matched to thalamocortical input (7)(8)(9).…”