A disinhibitory circuit motif and flexible information routing in the brain

Abstract

In the mammalian neocortex, an area typically receives inputs from, and projects to, dozens of other areas. Mechanisms are needed to flexibly route information to the right place at the right time, which we term 'pathway gating'. For instance, a region in your brain that receives signals from both visual and auditory pathways may want to 'gate in' the visual pathway while 'gating out' the auditory pathway when you try to read a book surrounded by people in a noisy café. In this review, we marshall experimental and computational evidence in support of a circuit mechanism for flexible pathway gating realized by a disinhibitory motif. Moreover, recent work shows an increasing preponderance of this disinhibitory motif from sensory areas to association areas of the mammalian cortex. Pathway input gating is briefly compared with alternative or complementary gating mechanisms. Predictions and open questions for future research on this puzzle about the complex brain system will be discussed.

Figure 1:

A disinhibitory circuit motif. (a) A neural circuit model for working memory with three types of inhibitory neurons, i.e. perisoma targeting, peridendrite-targeting, and interneuron-targeting neurons. Dendrite-targeting inhibitory neurons (blue) control the resistance to distractors (adapted from [9]). (b) The circuit diagram of PV, CB, and CR neurons. The connection probabilities between different types of neurons are measured in inferior temporal cortex of maca que monkey (adapted from [32]). (c) Number of CR, CB, and PV neurons in three subregions of the macaque monkey prefrontal cortex, showing that PV are not predominant among the three interneuron types in the prefrontal cortex. (adapted from [33]).

Figure 2:

A disinhibitory circuit motif for pathway gating. (a) The disinhibitory circuit diagram with PV, SST, and VIP neurons. (b) An area receives converging inputs from visual and auditory pathways. The control input selectively opens the gate for one pathway. (c) To open the gate for the visual pathway, the control input can target a subset of VIP and SST neurons, leading to disinhibition of dendrites targeted by the visual pathway (adapted from [26]).

Figure 3:

A cortical hierarchy based on SST/PV cell density ratio. Mouse cortical areas are ranked by the ratio between their PV and SST cell densities. Primary somatosensory areas are abundant in PV neurons, while prefrontal areas are dominated by SST neurons (adapted from [55]). The color code indicates the cortical subnetwork each area belongs to [5].

Figure 4:

Various mechanisms for information gating in the brain. Input gating can be achieved by dendrite-targeting interneurons that selectively control inputs to pyramidal dendrites. In the synchronous gating mechanism, communication between two areas depends on the degree of temporal synchrony of neural activity between the source and target areas. Recurrent gating mechanism involves selective integration of inputs based on context-dependent dynamics of the network. Output gating is instantiated with perisoma-targeting interneurons that specifically inhibit pyramidal neurons projecting to one pathway but not others. Gating may also involve subcortical structures, especially basal ganglia and thalamus.