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.

Keywords: attention; decision making; movement; normalization; orienting; population coding; saccades; vision.

Figure 1

Schematic representation of the brain, highlighting the location of the superior colliculus in two mammalian species, a monkey and a mouse (not drawn to scale). The dashed line indicates an axial cut through the colliculus to reveal the layers of the colliculus. Stratum griseum superficiale (SGS) and stratum opticum (SO) together comprise the visuosensory layers, and the stratum griseum intermediale (SGI) together with the deeper layers comprise the motor layers. The schematic on the right shows the known neuronal types within the colliculus and their projection patterns. Narrow-field vertical cells (blue) project to the lateral geniculate nucleus (LGN), and the wide-field vertical cells (green) project to the pulvinar. Output neurons of the motor layers (brown) project to the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) to control vertical eye movements and to the paramedian pontine reticular formation (PPRF) to control horizontal eye movements. The motor layers also project upstream to the medial dorsal nucleus of the thalamus (MD). Abbreviations: SAI, stratum album intermediale; SAP, stratum album profundum; SGP, stratum griseum profundum; SZ, stratum zonale.

Figure 2

(a) The map of saccadic eye movement space across the movement layers of the left superior colliculus as discovered by Robinson. Rostral is at the top and caudal is at the bottom. (b) The visual field representation corresponding to the left colliculus. Blue dots show locations of visual stimuli in visual space and correspondingly on the collicular map. Adapted from Robinson (1972).

Figure 3

Schematic representation of activity across the movement map of the superior colliculus during a simple task in which one differently colored stimulus is chosen as a target for a saccade. The circles on the top are the possible targets (red or green), and the maps below are heat maps in which warmer colors represent higher levels of neuronal activity. One could think of these hills of activity as likelihoods; a linear sum across all activity will naturally lead to a probability distribution of all possible saccades. The peak would be the most likely saccade, whereas the width of population distribution provides an implicit representation of the certainty of the saccade choice. Adapted from Kim & Basso (2008, .

Figure 4

The relative level of activity across the collicular map encodes saccadic eye movement choice. (a) Receiver operating characteristic (ROC) area and d′, two measures of discriminability, are plotted against the performance accuracy in a simple target selection task. The relative activity scales linearly with performance accuracy. (b) The same data are plotted as a function of saccade amplitude or distance to the saccade from the fixation point. (c) The same data are plotted as a function of saccade velocity. Discriminability correlates best with target choice and least with saccade parameters. From Kim & Basso (2008).

Figure 5

Distribution of terminals following an injection of biotinylated dextran amine (BDA) into the superior colliculus. Injection site shown in panels i, j,and k. Note denser terminal labeling in panels a–h rostral to the injection site, compared to panels i–s caudal to the injection site.

Figure 6

A role for the superior colliculus (SC) in attention. (a) Monkeys attended to one of four motion patches determined by a colored ring cue. One patch then changed its motion direction, and monkeys reported this change by making a saccade to a choice target (or pressing a button) corresponding to the change in motion direction. (b) Inactivation of the colliculus in the region of the colliculus representing the cue led to impaired detection at that location and increased responding to the foil. The inset shows the trial condition. Points falling along the dashed line indicate no change with activation. (c) Same as in panel b for the condition in which the foil appeared in the inactivated region. In this case, monkeys ignored it. Adapted with permission from Krauzlis et al. (2013).

Figure 7

Electrical stimulation of the colliculus changes decision criteria in predictable ways. Proportion of a Yes response is plotted as a function of decision difficulty (coherence). Panel a shows the results of priming with a visual stimulus, and panel b shows the results of priming with electrical stimulation of the motor layers of the colliculus. Blue shows the results with liberal priming, and orange shows the results with conservative priming. Black is baseline data with no priming or stimulation. n indicates the number of sessions averaged. From Crapse & Basso (2014).

Figure 8

Schematic illustration of the circuits in the avian tectum thought to control attention. Red shows inhibitory connections and blue shows excitatory connections. Numbers indicate tectal layers in the bird. Arrowheads show terminals, whereas ovals, pentagons, and triangles show neuronal cell bodies. Abbreviations: Ipc, nucleus isthmus pars parvocellularis; Ipm, nucleus isthmus pars magnocellularis.

Figure 9

Normalization in a collicular slice. (a) Image of the colliculus through the microscope during the experiment showing the two electrodes. (b) Activation of one site results in a population membrane depolarization in the motor layers that extends to the visuosensory layers. The magnitude of the depolarization is indicated by the heat map with warmer colors indicating more depolarization. (c) Same as in panel b for site 2. (d) Population response to dual-site stimulation. (e) Population responses fitted with Gaussians to extract the center and amplitude of the responses. Circles show data, and lines show fits. (f) Linear sum model prediction (ΔI/I) is plotted against the actual response evoked with two sites of stimulation (ΔI/I). Points falling above the line indicate that the linear sum does not predict the dual-site response. Adapted with permission from Vokoun et al. (2014). Abbreviations: I/I, delta intensity/intensity; CCD, charge-coupled device; SGI, stratum griseum intermediale; SGS, stratum griseum superficiale; SO, stratum opticum.