An integrative role for the superior colliculus in selecting targets for movements

Abstract

A fundamental goal of systems neuroscience is to understand the neural mechanisms underlying decision making. The midbrain superior colliculus (SC) is known to be central to the selection of one among many potential spatial targets for movements, which represents an important form of decision making that is tractable to rigorous experimental investigation. In this review, we first discuss data from mammalian models-including primates, cats, and rodents-that inform our understanding of how neural activity in the SC underlies the selection of targets for movements. We then examine the anatomy and physiology of inputs to the SC from three key regions that are themselves implicated in motor decisions-the basal ganglia, parabrachial region, and neocortex-and discuss how they may influence SC activity related to target selection. Finally, we discuss the potential for methodological advances to further our understanding of the neural bases of target selection. Our overarching goal is to synthesize what is known about how the SC and its inputs act together to mediate the selection of targets for movements, to highlight open questions about this process, and to spur future studies addressing these questions.

Keywords: decision making; laterodorsal tegmental nucleus; motor planning; pedunculopontine tegmental nucleus; substantia nigra.

Fig. 1.

Input to the superior colliculus (SC) from key regions underlying sensorimotor decision making that are the focus of this review. A: schematic of anatomical projections and information flow. While the SC receives input from numerous regions, we focus here on the glutamatergic input from the neocortex, cholinergic input from the pedunculopontine tegmental nucleus (PPTg) and laterodorsal tegmental nucleus (LDTg), and GABAergic input from the substantia nigra pars reticulata (SNr). This input influences intrinsic processing in the SC that may underlie the selection of targets for movements, which are then coordinated and initiated via SC output to premotor nuclei in the brain stem and spinal cord. B: schematic of synaptic inputs to the deep subdivision of the SC from the above regions. Notably, axons projecting from regions that may “drive” SC activity (e.g., neocortex) are thicker and synapse more proximal to the soma than axons projecting from regions that may “modulate” SC activity (e.g., SNr, PPTg/LDTg).

Fig. 2.

Examples of recordings from the SC of rodents performing behavioral tasks requiring the selection of a target for movement. A: generalized schematic of the events in the task during which recordings in B and in Fig. 4 were taken. The rodent enters the central port, receives an odor associated with reward at one side, waits for a go signal, and orients to a port for a water reward. B: smoothed peristimulus time histograms (mean ± SE) for 2 SC neurons recorded in a rat performing the task shown in A. Black, activity associated with selecting contralateral target; gray, activity associated with selecting ipsilateral target. Stimulus presentation is shown as the gradient along the x-axis, and go signal is shown as a vertical dotted line. Some neurons exhibit higher activity preceding movement to contraversive target (as at top), and some exhibit higher activity preceding movement to ipsiversive target (as at bottom). Data from Felsen and Mainen (2012). For comparable data recorded in primates in a similar experimental paradigm, see Horwitz and Newsome (2001a).

Fig. 3.

Difficulty dependence of the behavioral effect of manipulating SC activity. A: unilateral channelrhodopsin-2 (ChR2)-mediated optical activation in the SC has a greater effect (contraversive shift) on hard trials (small odor mixture contrasts) than easy trials (large odor contrast). Data from Stubblefield et al. (2013). B: unilateral inhibition via muscimol infusion into the SC has a greater effect (ipsiversive shift) on hard trials than easy trials. Saline was delivered during Pre and Recovery sessions. Data from Felsen and Mainen (2008). For comparable data collected in primates in a similar experimental paradigm, see McPeek and Keller (2004).

Fig. 4.

Examples of neural recordings from rodents performing behavioral tasks requiring the selection of a target for movement. A: smoothed peristimulus time histograms (mean ± SE) for 2 SNr neurons recorded in a mouse performing the task shown in Fig. 2A. Black, activity associated with selecting contralateral target; gray, activity associated with selecting ipsilateral target. Stimulus presentation is shown as the gradient along the x-axis, and go signal is shown as a vertical dotted line. Some neurons exhibit higher activity preceding movement to contraversive target (as at top), and some exhibit higher activity preceding movement to ipsiversive target (as at bottom). Data from Lintz and Felsen (2014). B: as in A, for 2 mouse PPTg neurons. Data from Thompson and Felsen (2013). C: as in A, for 2 rat frontal orienting field (FOF) neurons. Rat FOF is thought to be homologous to primate frontal eye field (FEF). In this task, target selection was cued by an auditory rather than olfactory stimulus. Data from Erlich et al. (2011). For comparable data recorded in primates in a similar experimental paradigm, see Handel and Glimcher (1999) (SNr), Okada and Kobayashi (2009) (PPTg), and Sommer and Wurtz (2000) (FEF).