Circuits for Action and Cognition: A View from the Superior Colliculus

Abstract

The superior colliculus is one of the most well-studied structures in the brain, and with each new report, its proposed role in behavior seems to increase in complexity. Forty years of evidence show that the colliculus is critical for reorienting an organism toward objects of interest. In monkeys, this involves saccadic eye movements. Recent work in the monkey colliculus and in the homologous optic tectum of the bird extends our understanding of the role of the colliculus in higher mental functions, such as attention and decision making. In this review, we highlight some of these recent results, as well as those capitalizing on circuit-based methodologies using transgenic mice models, to understand the contribution of the colliculus to attention and decision making. The wealth of information we have about the colliculus, together with new tools, provides a unique opportunity to obtain a detailed accounting of the neurons, circuits, and computations that underlie complex behavior.

Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse

“…In future work, it will be also be fruitful to further explore how the cell types accessed here contribute to other natural visually-guided behaviors in the mouse such as active predator avoidance, navigation or novel object exploration (Cooper et al, 1998;Park et al, 2018) . Importantly, it is also well established that SC, particularly in higher mammals is required for more complex visuomotor and even cognitive functions, such as spatial selective attention (for recent reviews see (Basso and May, 2017;Krauzlis et al, 2013) . This study begins to clarify our understanding of SC visual processing in this context by identifying specific cell types that are differentially required for aspects of visually-guided locomotor orienting.…”

“…The SC is a laminated structure, with the superficial SC (sSC) receiving multiple sources of visual input, while the intermediate and deeper layers receive multimodal sensory input, project to a broad range of targets and provide motor output (May, 2006) . Work in rodents and other species studying the physiological properties and visual stimulus encoding of sSC cells has advanced our detailed understanding of structure-function relationships of specific neuron types in the mammalian SC (Basso and May, 2017;Cang et al, 2018;Ito and Feldheim, 2018;Oliveira and Yonehara, 2018) . In particular, the classically defined wide-field (WF) and narrow-field (NF) vertical cell types (Ramón y, Cajal S Translated by Swanson N, 1995) have distinct functional and anatomical properties that indicate they may contribute to unique aspects of early visual processing to drive natural approach behaviors.…”

Monosynaptic Inputs to Excitatory and Inhibitory Neurons of the Intermediate and Deep Layers of the Superior Colliculus

“…Our findings that different populations of SC neurons receive unique patterns of input argue against the view of the SCid as a simple relay and instead support the idea that intrinsic processing gives rise to SCid computations for orienting behavior. Studies examining SCid activity when multiple targets are present (Basso and Wurtz, 1997;McPeek and Keller, 2004;Li and Basso, 2005;Felsen and Mainen, 2008) support a model of SCid function whereby a "competition" takes place between two or more active foci within the colliculus (Basso and May, 2017). While this competition could simply reflect differences in the activity level of different inputs, local inhibitory connectivity within and between the two SCids (Takahashi et al, 2005(Takahashi et al, , 2007(Takahashi et al, , 2010Isa and Hall, 2009;Sooksawate et al, 2011;Ghitani et al, 2014) suggests that active intrinsic SCid processes may be at work.…”

“…The SC is critical for a wide range of functions, ranging from spatial attention to multisensory integration to adaptive behavioral responses (Dean et al, 1989;Stein and Stanford, 2008;Gandhi and Katnani, 2011;Krauzlis et al, 2013;Basso and May, 2017). Its intricate internal circuitry is organized into seven cytoarchitechtonically-defined layers composed of excitatory and inhibitory neurons each with diverse projection patterns (Edwards, 1977;Mize, 1992;Olivier et al, 1998Olivier et al, , 2000Pettit et al, 1999;Takahashi et al, 2005Takahashi et al, , 2007Takahashi et al, , 2010Isa and Hall, 2009;Sooksawate et al, 2011;Ghitani et al, 2014).…”

“…The superior colliculus (SC) is a highly conserved midbrain structure critical for orienting behavior (Basso and May, 2017), as well as other associated functions such as spatial attention (Krauzlis et al, 2013) and multisensory integration (Stein and Stanford, 2008). The SC is organized into a superficial visual layer, which receives projections from the retina (Apter, 1945) and descending inputs from the neocortex (Kawamura et al, 1974), and intermediate and deep layers (SCid) that receive widespread input from several cortical and subcortical regions (Sparks and Hartwich-Young, 1989).…”