Correlates of Perceptual Learning in an Oculomotor Decision Variable

Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6074, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 03/2009; 29(7):2136-50. DOI: 10.1523/JNEUROSCI.3962-08.2009
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In subjects trained extensively to indicate a perceptual decision with an action, neural commands that generate the action can represent the process of forming the decision. However, it is unknown whether this representation requires overtraining or reflects a more general link between perceptual and motor processing. We examined how perceptual processing is represented in motor commands in naive monkeys being trained on a demanding perceptual task, as they first establish the sensory-motor association and then learn to form more accurate perceptual judgments. The task required the monkeys to decide the direction of random-dot motion and respond with an eye movement to one of two visual targets. Using electrically evoked saccades, we examined oculomotor commands that developed during motion viewing. Throughout training, these commands tended to reflect both the subsequent binary choice of saccade target and the weighing of graded motion evidence used to arrive at that choice. Moreover, these decision-related oculomotor signals, along with the time needed to initiate the voluntary saccadic response, changed steadily as training progressed, approximately matching concomitant improvements in behavioral sensitivity to the motion stimulus. Thus, motor circuits may have general access to perceptual processing used to select between actions, even without extensive training. The results also suggest a novel candidate mechanism for some forms of perceptual learning, in which the brain learns rapidly to treat a perceptual decision as a problem of action selection and then over time to use sensory input more effectively to guide the selection process.

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Available from: Sharath Bennur, Jun 06, 2015
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    • "In particular , the signal encodes each quantum of evidence in a ramp-like fashion and distinguishes the quantum supporting from the quantum contradicting the decision to choose a button press. Studies of decision-related neural dynamics in non-human primates have been subjected to the criticism that decision variables are encoded in oculomotor circuits (Gold and Shadlen, 2000, 2002; Horwitz and Newsome, 1999; Kable and Glimcher, 2009; Platt and Glimcher, 1999) simply because animals were conditioned to map perceptual decisions onto motor outputs through extensive training (Connolly et al., 2009). Our finding argues against this lingering criticism by showing that a perceptual decision variable is represented in motor circuits of the brain even when subjects are not extensively trained in a decision task. "
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    ABSTRACT: We often make decisions based on sensory evidence that is accumulated over a period of time. How the evidence for such decisions is represented in the brain and how such a neural representation is used to guide a subsequent action are questions of considerable interest to decision sciences. The neural correlates of developing perceptual decisions have been thoroughly investigated in the oculomotor system of macaques who communicated their decisions using an eye movement. It has been found that the evidence informing a decision to make an eye movement is in part accumulated within the same oculomotor circuits that signal the upcoming eye movement. Recent evidence suggests that the somatomotor system may exhibit an analogous property for choices made using a hand movement. To investigate this possibility, we engaged humans in a decision task in which they integrated discrete quanta of sensory information over a period of time and signaled their decision using a hand movement or an eye movement. The discrete form of the sensory evidence allowed us to infer the decision variable on which subjects base their decision on each trial and to assessthe neural processes related to each quantum of the incoming decision evidence. We found that a low-frequency electrophysiological signal recorded over centroparietal regions strongly encodes the decision variable inferred in this task, and that it does so specifically for hand movement choices. The signal ramps up with a rate that is proportional to the decision variable, remains graded by the decision variable throughout the delay period, reaches a common peak shortly before a hand movement, and falls off shortly after the hand movement. Furthermore, the signal encodes the polarity of each evidence quantum, with a short latency, and retains the response level over time. Thus, this neural signal shows properties of evidence accumulation. These findings suggest that the decision-related effects observed in the oculomotor system of the monkey during eye movement choices may share the same basic properties with the decision-related effects in the somatomotor system of humans during hand movement choices.
    NeuroImage 07/2013; 83. DOI:10.1016/j.neuroimage.2013.06.085 · 6.36 Impact Factor
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    • "To date, a large number of functional neuroimaging studies have adopted task-based experimental designs to investigate the neural correlates of stimulus–response associations in humans (Egner, 2007) and non-human primates (Connolly et al., 2009). Despite the differences in experimental designs, several studies have provided consistent evidence for an implementation of these processes in a bilateral fronto-parietal network. "
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    ABSTRACT: Bidirectional integration between sensory stimuli and contextual framing is fundamental to action control. Stimuli may entail context-dependent actions, while temporal or spatial characteristics of a stimulus train may establish a contextual framework for upcoming stimuli. Here we aimed at identifying core areas for stimulus-context integration and delineated their functional connectivity (FC) using meta-analytic connectivity modeling (MACM) and analysis of resting-state networks. In a multi-study conjunction, consistently increased activity under higher demands on stimulus-context integration was predominantly found in the right temporo-parietal junction (TPJ), which represented the largest cluster of overlap and was thus used as the seed for the FC analyses. The conjunction between task-dependent (MACM) and task-free (resting state) FC of the right TPJ revealed a shared network comprising bilaterally inferior parietal and frontal cortices, anterior insula, premotor cortex, putamen and cerebellum, i.e., a 'ventral' action/attention network. Stronger task-dependent (vs. task-free) connectivity was observed with the pre-SMA, dorsal premotor cortex, intraparietal sulcus, basal ganglia and primary sensori motor cortex, while stronger resting-state (vs. task-dependent) connectivity was found with the dorsolateral prefrontal and medial parietal cortex. Our data provide strong evidence that the right TPJ may represent a key region for the integration of sensory stimuli and contextual frames in action control. Task-dependent associations with regions related to stimulus processing and motor responses indicate that the right TPJ may integrate 'collaterals' of sensory processing and apply (ensuing) contextual frames, most likely via modulation of preparatory loops. Given the pattern of resting-state connectivity, internal states and goal representations may provide the substrates for the contextual integration within the TPJ in the absence of a specific task.
    NeuroImage 02/2012; 60(4):2389-98. DOI:10.1016/j.neuroimage.2012.02.037 · 6.36 Impact Factor
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    ABSTRACT: We recently showed that improved perceptual performance on a visual motion direction-discrimination task corresponds to changes in how an unmodified sensory representation in the brain is interpreted to form a decision that guides behavior. Here we found that these changes can be accounted for using a reinforcement-learning rule to shape functional connectivity between the sensory and decision neurons. We modeled performance on the basis of the readout of simulated responses of direction-selective sensory neurons in the middle temporal area (MT) of monkey cortex. A reward prediction error guided changes in connections between these sensory neurons and the decision process, first establishing the association between motion direction and response direction, and then gradually improving perceptual sensitivity by selectively strengthening the connections from the most sensitive neurons in the sensory population. The results suggest a common, feedback-driven mechanism for some forms of associative and perceptual learning.
    Nature Neuroscience 05/2009; 12(5):655-63. DOI:10.1038/nn.2304 · 16.10 Impact Factor
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