Distinct neural mechanisms construct classical versus extraclassical inhibitory surrounds in an inhibitory nucleus in the midbrain attention network.

Inhibitory neurons in the midbrain spatial attention network, called isthmi pars magnocellularis (Imc), control stimulus selection by the sensorimotor and attentional hub, the optic tectum (OT). Here, we investigate in the barn owl how classical as well as extraclassical (global) inhibitory surrounds of Imc receptive fields (RFs), fundamental units of Imc computational function, are constructed. We find that focal, reversible blockade of GABAergic input onto Imc neurons disconnects their extraclassical inhibitory surrounds, but leaves intact their classical inhibitory surrounds. Subsequently, with paired recordings and iontophoresis, first at spatially aligned site-pairs in Imc and OT, and then, at mutually distant site-pairs within Imc, we demonstrate that classical inhibitory surrounds of Imc RFs are inherited from OT, but their extraclassical inhibitory surrounds are constructed within Imc. These results reveal key design principles of the midbrain spatial attention circuit and highlight the critical importance of competitive interactions within Imc for its operation.

Categorical Signaling of the Strongest Stimulus by an Inhibitory Midbrain Nucleus.

The nucleus isthmi pars magnocellularis (Imc), a group of inhibitory neurons in the midbrain tegmentum, is a critical component of the spatial selection network in the vertebrate midbrain. It delivers long-range inhibition among different portions of the space map in the optic tectum (OT), thereby mediating stimulus competition in the OT. Here, we investigate the properties of relative strength-dependent competitive interactions within the Imc, in barn owls of both sexes. We find that when Imc neurons are presented simultaneously with one stimulus inside the receptive field and a second, competing stimulus outside, they exhibit gradual or switch-like response profiles as a function of relative stimulus strength. They do so both when the two stimuli are of the same sensory modality (both visual) or of different sensory modalities (visual and auditory). Moreover, Imc neurons signal the strongest stimulus in a dynamically flexible manner, indicating that Imc responses reflect an online comparison between the strengths of the competing stimuli. Notably, Imc neurons signal the strongest stimulus more categorically, and earlier than the OT. Paired recordings at spatially aligned sites in the Imc and OT reveal that although some properties of stimulus competition, such as the bias of competitive response profiles, are correlated, others such as the steepness of response profiles, are set independently. Our results demonstrate that the Imc is itself an active site of competition, and may be the first site in the midbrain selection network at which stimulus competition is resolved.SIGNIFICANCE STATEMENT This work sheds light on the functional properties of a small group of inhibitory neurons in the vertebrate midbrain that play a key part in how the brain selects a target among competitors. A better understanding of the functioning of these neurons is an important building block for the broader understanding of how distracters are suppressed, and of spatial attention and its dysfunction.

Spatial Dependence of Stimulus Competition in the Avian Nucleus Isthmi Pars Magnocellularis.

The nucleus isthmi pars magnocellularis (Imc) is a group of specialized inhibitory neurons in the midbrain tegmentum, thought to be conserved across vertebrate classes. Past anatomical work in reptiles has suggested a role for it in stimulus selection, which has been supported by recent studies in avians. Additionally, focal inactivation of Imc neurons is known to abolish all competitive interactions in the optic tectum (OT; SC in mammals), a midbrain sensorimotor hub that is critical for the control of spatial attention, thereby revealing a key role for Imc in stimulus selection. However, the functional properties of Imc neurons are not well understood. Here, with electrophysiological experiments in the barn owl Imc, we show that Imc neurons themselves exhibit signatures of stimulus competition. Distant competing stimuli outside the spatial receptive field (RF) suppressed powerfully, and divisively, the responses of Imc neurons to stimuli inside the RF, and did so from all tested locations along the elevation as well as azimuth. Notably, this held true even for locations encoded by the opposite side of the brain from the one containing the recording site. This global divisive inhibition operated independently of the sensory modality of the competing stimulus. Thus, the Imc not only supplies inhibition to the OT to support competition there, but may itself be an active site of stimulus competition. These results from experiments in the barn owl shed light on the functional properties of a vital node in the vertebrate midbrain selection network.