Representation of an Abstract Perceptual Decision in Macaque Superior Colliculus

Stanford University, Palo Alto, California, United States
Journal of Neurophysiology (Impact Factor: 2.89). 06/2004; 91(5):2281-96. DOI: 10.1152/jn.00872.2003
Source: PubMed


We recorded from neurons in the intermediate and deep layers of the superior colliculus (SC) while monkeys performed a novel direction discrimination task. In contrast to the task we used previously, the new version required the monkey to dissociate perceptual judgments from preparation to execute specific operant saccades. The monkey discriminated between 2 opposed directions of motion in a random-dot motion stimulus and was required to maintain the decision in memory throughout a delay period before the target of the required operant saccade was revealed. We hypothesized that perceptual decisions made in this paradigm would be represented in an "abstract" or "categorical" form within the brain, probably in the frontal cortex, and that decision-related neural activity would be eliminated from spatially organized preoculomotor structures such as the SC. To our surprise, however, a small population of neurons in the intermediate and deep layers of the SC fired in a choice-specific manner early in the trial well before the monkey could plan the operant saccade. Furthermore, the representation of the decision during the delay period appeared to be spatial: the active region in the SC map corresponded to the region of space toward which the perceptually discriminated stimulus motion flowed. Electrical microstimulation experiments suggested that these decision-related SC signals were not merely related to covert saccade planning. We conclude that monkeys may employ, in part, a spatially referenced mnemonic strategy for representing perceptual decisions, even when an abstract, categorical representation might appear more likely a priori.

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    • "Previous studies on the encoding of abstract choices Previous monkey electrophysiology studies have demonstrated signals reflecting abstract choices in the superior colliculus, supplementary eye field (Horwitz et al., 2004), and the lateral intraparietal area (Bennur and Gold, 2011). Although choices can accurately be predicted from neuronal responses in the frontal eye field (Kim and Shadlen, 1999), this region only seems to be involved in the decision process when a motor response (saccade) is planned concomitantly (Gold and Shadlen, 2000, 2003). "
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    ABSTRACT: Perceptual decision-making entails the transformation of graded sensory signals into categorical judgments. Often, there is a direct mapping between these judgments and specific motor responses. However, when stimulus-response mappings are fixed, neural activity underlying decision-making cannot be separated from neural activity reflecting motor planning. Several human neuroimaging studies have reported changes in brain activity associated with perceptual decisions. Nevertheless, to date it has remained unknown where and how specific choices are encoded in the human brain when motor planning is decoupled from the decision process. We addressed this question by having subjects judge the direction of motion of dynamic random dot patterns at various levels of motion strength while measuring their brain activity with fMRI. We used multivariate decoding analyses to search the whole brain for patterns of brain activity encoding subjects' choices. To decouple the decision process from motor planning, subjects were informed about the required motor response only after stimulus presentation. Patterns of fMRI signals in early visual and inferior parietal cortex predicted subjects' perceptual choices irrespective of motor planning. This was true across several levels of motion strength and even in the absence of any coherent stimulus motion. We also found that the cortical distribution of choice-selective brain signals depended on stimulus strength: While visual cortex carried most choice-selective information for strong motion, information in parietal cortex decreased with increasing motion coherence. These results demonstrate that human visual and inferior parietal cortex carry information about the visual decision in a more abstract format than can be explained by simple motor intentions. Both brain regions may be differentially involved in perceptual decision-making in the face of strong and weak sensory evidence.
    NeuroImage 08/2012; 63(3):1393-403. DOI:10.1016/j.neuroimage.2012.08.027 · 6.36 Impact Factor
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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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    • "When a choice is ultimately communicated through an action, say to move the eyes, the evolving decision process has its neural correlate in the firing rates of neurons in areas of the brain that play a role in planning eye movements (Schall, 2001; Sugrue et al., 2005; Gold and Shadlen, 2007; Glimcher et al., 2008). These and other findings suggest that the oculomotor system receives a continuous flow of information that could help to prepare an eventual action (Bichot et al., 2001; Gold and Shadlen, 2001; Horwitz et al., 2004). Such continuous flow (Eriksen and Schultz, 1979) might seem like a peculiar design for a brain because it challenges the common-sense notion that decisions concern information bearing on propositions and not the actions that ensue as a result of the decision. "
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    ABSTRACT: Both decision making and sensorimotor control require real-time processing of noisy information streams. Historically these processes were thought to operate sequentially: cognitive processing leads to a decision, and the outcome is passed to the motor system to be converted into action. Recently, it has been suggested that the decision process may provide a continuous flow of information to the motor system, allowing it to prepare in a graded fashion for the probable outcome. Such continuous flow is supported by electrophysiology in nonhuman primates. Here we provide direct evidence for the continuous flow of an evolving decision variable to the motor system in humans. Subjects viewed a dynamic random dot display and were asked to indicate their decision about direction by moving a handle to one of two targets. We probed the state of the motor system by perturbing the arm at random times during decision formation. Reflex gains were modulated by the strength and duration of motion, reflecting the accumulated evidence in support of the evolving decision. The magnitude and variance of these gains tracked a decision variable that explained the subject's decision accuracy. The findings support a continuous process linking the evolving computations associated with decision making and sensorimotor control.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 02/2012; 32(7):2276-86. DOI:10.1523/JNEUROSCI.5273-11.2012 · 6.34 Impact Factor
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