Saccade Target Selection in the Superior Colliculus: A Signal Detection Theory Approach

Department of Physiology, University of Wisconsin-Madison, School of Medicine and Public Health, Madison, Wisconsin 53706, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 04/2008; 28(12):2991-3007. DOI: 10.1523/JNEUROSCI.5424-07.2008
Source: PubMed

ABSTRACT How the brain selects one action from among multiple options is unknown. A main tenet of signal detection theory (SDT) is that sensory stimuli are represented as noisy information channels. Therefore, the accuracy of selection might be predicted by how well neuronal activity representing alternatives can be distinguished. Here, we apply an SDT framework to a motor system by recording from superior colliculus (SC) neurons during performance of a color, oddball selection task. We recorded from sets of four neurons simultaneously, each of the four representing one of the four possible targets. Because the electrode placement constrained the position of the stimuli in the visual field, the stimulus arrangement varied across experiments. This variability in stimulus arrangement led to variability in choices allowing us to explore the relationship between SC neuronal activity and performance accuracy. SC target neurons had higher levels of discharge than SC distractor neurons in subsets of trials when selection performance was very accurate. In subsets of trials when performance was poor, the discharge level decreased in target neurons and increased in distractor neurons. Accurate performance was associated with larger separations between neuronal activity from targets and distractors as quantified by the receiver operating characteristic (ROC) area and d' (an index of discriminability). Poorer performance was associated with less separation of target and distractor neuronal activity. ROC area and d' scaled approximately linearly with performance accuracy. Furthermore, ROC area and d' increased as saccade onset approached. Together, the results indicate that SC buildup neuronal activity signals the saccadic eye movement decision.

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Available from: Byounghoon Kim, Sep 28, 2015
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    • "All of the results described above were based entirely on modulation of discharge rates of individual neurons. It is clear, though, that saccade target selection is accomplished by pools of neurons [148] [174] [175] and probably entails more than just modulation of spike rate because cooperation and competition between pairs of neurons is modulated during target selection [176]. Indeed, correlation in discharge rates of FEF neurons over longer time scales has been reported even before stimulus presentation [177]. "
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    ABSTRACT: Primate vision is served by rapid shifts of gaze called saccades. This review will survey current knowledge and particular problems concerning the neural control and guidance of gaze shifts.
    10/2013; 2013(9):752384. DOI:10.1155/2013/752384
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    • "In fact, several recent studies in primates have proposed that SC activity reflects decision-related variables, suggesting that it is directly involved in saccadic decisions (Horwitz et al. 2004; Kim and Basso 2008; Lee and Keller 2006). However, an outstanding question is whether the SC is involved only in motor decisions based on a modality that it explicitly represents—visual , auditory, or somatosensory— or whether it contributes to a wider class of decisions. "
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    ABSTRACT: Making decisions about future actions is a fundamental function of the nervous system. Classical theories hold that separate sets of brain regions are responsible for selecting and implementing an action. Traditionally, action selection has been considered the domain of high-level regions, such as the prefrontal cortex, whereas action generation is thought to be carried out by dedicated cortical and subcortical motor regions. However, increasing evidence suggests that the activity of individual neurons in cortical motor structures reflects abstract properties of "decision variables" rather than conveying simple motor commands. Less is known, though, about the role of subcortical structures in decision making. In particular, the superior colliculus (SC) is critical for planning and initiating visually guided, gaze-displacing movements and selecting visual targets, but whether and how it contributes more generally to sensorimotor decisions are unclear. Here, we show that the SC is intimately involved in orienting decisions based on odor cues, even though the SC does not explicitly process olfactory stimuli. Neurons were recorded from the intermediate and deep SC layers in rats trained to perform a delayed-response, odor-cued spatial choice task. SC neurons commonly fired well in advance of movement initiation, predicting the chosen direction nearly 1 s before movement. Moreover, under conditions of sensory uncertainty, SC activity varied with task difficulty and reward outcome, reflecting the influence of decision variables on the intercollicular competition thought to underlie orienting movements. These results indicate that the SC plays a more general role in decisions than previously appreciated, extending beyond visuomotor functions.
    Journal of Neurophysiology 04/2012; 108(1):135-47. DOI:10.1152/jn.01181.2011 · 2.89 Impact Factor
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    • "Therefore, the activity difference between the two hemispheres of SC might restrict the reaction toward peripheral targets. This assumption is supported by a recent study suggesting that the activity difference among different populations of SC neurons reflects the certainty of direction choice in primates [85]. "
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    ABSTRACT: Animals can make faster behavioral responses to multisensory stimuli than to unisensory stimuli. The superior colliculus (SC), which receives multiple inputs from different sensory modalities, is considered to be involved in the initiation of motor responses. However, the mechanism by which multisensory information facilitates motor responses is not yet understood. Here, we demonstrate that multisensory information modulates competition among SC neurons to elicit faster responses. We conducted multiunit recordings from the SC of rats performing a two-alternative spatial discrimination task using auditory and/or visual stimuli. We found that a large population of SC neurons showed direction-selective activity before the onset of movement in response to the stimuli irrespective of stimulation modality. Trial-by-trial correlation analysis showed that the premovement activity of many SC neurons increased with faster reaction speed for the contraversive movement, whereas the premovement activity of another population of neurons decreased with faster reaction speed for the ipsiversive movement. When visual and auditory stimuli were presented simultaneously, the premovement activity of a population of neurons for the contraversive movement was enhanced, whereas the premovement activity of another population of neurons for the ipsiversive movement was depressed. Unilateral inactivation of SC using muscimol prolonged reaction times of contraversive movements, but it shortened those of ipsiversive movements. These findings suggest that the difference in activity between the SC hemispheres regulates the reaction speed of motor responses, and multisensory information enlarges the activity difference resulting in faster responses.
    PLoS ONE 09/2011; 6(9):e25283. DOI:10.1371/journal.pone.0025283 · 3.23 Impact Factor
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