The indirect route

There has been a bit of mystery around how different areas of the cortex initiate shared synchrony or seem to pass information between them.

A paper from a few years back (Poulet, Fernandez, Crochet, Peterson; Thalamic control of cortical states; Nature 2012) showed that the activity of the whiskers of mice affected the state of activity in the cortex. How did the whiskers affect the whole cortex rather than just the whisker sensory area? It was via the thalamus shown by producing the effect without whisker activity by stimulation of thalamus alone.

We investigated the impact of thalamus on ongoing cortical activity in the awake, behaving mouse. We demonstrate that the desynchronized cortical state during active behavior is driven by a centrally generated increase in thalamic action potential firing, which can also be mimicked by optogenetic stimulation of the thalamus. The thalamus therefore is key in controlling cortical states.”

But that was a very general demonstration of thalamic control of large areas of the cortex. What about more specific action? A more recent paper, which uses a wide array of methods, shows a specific case (Wimmer, Schmitt, Davidson, Nakajima, Desseroth, Halassa; Thalamic control of sensory selection in divided attention; Nature 2016).

From their introduction: “Thirty years ago, Francis Crick proposed that the TRN (thalamic reticular nucleus) functions as a searchlight, directing the internal spotlight of attention to thalamo-cortical circuits that process ongoing behavioral demands. Due to technical limitations, this transformative model has been difficult to test, particularly under conditions where the attentional spotlight shifts. Our study combined novel and established technology to provide mechanistic details for Crick’s ‘searchlight hypothesis’. As such, we have taken important step in understanding the circuit mechanisms of sensory selection.”

The object/s of attention can come from bottom-up or top-down processes. In other words they can be triggered by perception or by cognitive and motor demands; triggered by external events or internal tasks. Top-down demands for attention to specific targets appear to originate in the frontal cortex and travel to specific areas of the sensory cortex making them more active. This paper shows that the information travels from the pre-frontal cortex to the appropriate sensory cortex area by way of the thalamus, via the appropriate part of the thalamic reticular nucleus.

Here is their abstract : “How the brain selects appropriate sensory inputs and suppresses distractors is a central unsolved mystery in neuroscience. Given the well-established role of prefrontal cortex (PFC) in executive function, its interactions with sensory cortical areas during attention have been hypothesized to control sensory selection. To test this idea and more generally dissect the circuits underlying sensory selection, we developed a cross-modal divided attention task in mice enabling genetic access to this cognitive process. By optogenetically perturbing PFC function in a temporally- precise window, the ability of mice to appropriately select between conflicting visual and auditory stimuli was diminished. Surprisingly, equivalent sensory thalamo-cortical manipulations showed that behavior was causally dependent on PFC interactions with sensory thalamus, not cortex. Consistent with this notion, we found neurons of the visual thalamic reticular nucleus (visTRN) to exhibit PFC-dependent changes in firing rate predictive of the modality selected. visTRN activity was causal to performance as confirmed via subnetwork-specific bi-directional optogenetic manipulations. Through a combination of electrophysiology and intracellular chloride photometry, we demonstrated that visTRN dynamically controls visual thalamic gain through feedforward inhibition. Combined, our experiments introduce a new subcortical model of sensory selection, where prefrontal cortex biases thalamic reticular subnetworks to control thalamic sensory gain, selecting appropriate inputs for further processing.

It is worth considering the idea that most of the information flow from one part of the cortex to another, where there is no clear, direct nerve tract, is actually traveling by way of the thalamus.

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