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      Orbitofrontal Cortex Value Signals Depend on Fixation Location during Free Viewing

      , ,
      Neuron
      Elsevier BV

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          Abstract

          <p id="P1">In the natural world, monkeys and humans judge the economic value of numerous competing stimuli by moving their gaze from one object to another, in a rapid series of eye movements. This suggests that the primate brain processes value serially, and that value-coding neurons may be modulated by changes in gaze. To test this hypothesis, we presented monkeys with value-associated visual cues, and took the unusual step of allowing unrestricted free viewing while we recorded neurons in the orbitofrontal cortex (OFC). By leveraging natural gaze patterns, we found that a large proportion of OFC cells encode gaze location, and that in some cells, value coding is amplified when subjects fixate near the cue. These findings provide the first cellular-level mechanism for previously documented behavioral effects of gaze on valuation, and suggest a major role for gaze in neural mechanisms of valuation and decision-making under ecologically realistic conditions. </p><p id="P2">McGinty et al. show that value signals in primate orbitofrontal cortex are driven by moment-to-moment changes in gaze location during natural free viewing. This surprisingly dynamic value code may play a key role in everyday decision-making and other motivated behaviors. </p>

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          Most cited references39

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          Self-control in decision-making involves modulation of the vmPFC valuation system.

          Every day, individuals make dozens of choices between an alternative with higher overall value and a more tempting but ultimately inferior option. Optimal decision-making requires self-control. We propose two hypotheses about the neurobiology of self-control: (i) Goal-directed decisions have their basis in a common value signal encoded in ventromedial prefrontal cortex (vmPFC), and (ii) exercising self-control involves the modulation of this value signal by dorsolateral prefrontal cortex (DLPFC). We used functional magnetic resonance imaging to monitor brain activity while dieters engaged in real decisions about food consumption. Activity in vmPFC was correlated with goal values regardless of the amount of self-control. It incorporated both taste and health in self-controllers but only taste in non-self-controllers. Activity in DLPFC increased when subjects exercised self-control and correlated with activity in vmPFC.
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            The importance of mixed selectivity in complex cognitive tasks.

            Single-neuron activity in the prefrontal cortex (PFC) is tuned to mixtures of multiple task-related aspects. Such mixed selectivity is highly heterogeneous, seemingly disordered and therefore difficult to interpret. We analysed the neural activity recorded in monkeys during an object sequence memory task to identify a role of mixed selectivity in subserving the cognitive functions ascribed to the PFC. We show that mixed selectivity neurons encode distributed information about all task-relevant aspects. Each aspect can be decoded from the population of neurons even when single-cell selectivity to that aspect is eliminated. Moreover, mixed selectivity offers a significant computational advantage over specialized responses in terms of the repertoire of input-output functions implementable by readout neurons. This advantage originates from the highly diverse nonlinear selectivity to mixtures of task-relevant variables, a signature of high-dimensional neural representations. Crucially, this dimensionality is predictive of animal behaviour as it collapses in error trials. Our findings recommend a shift of focus for future studies from neurons that have easily interpretable response tuning to the widely observed, but rarely analysed, mixed selectivity neurons.
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              Neurons in the orbitofrontal cortex encode economic value.

              Economic choice is the behaviour observed when individuals select one among many available options. There is no intrinsically 'correct' answer: economic choice depends on subjective preferences. This behaviour is traditionally the object of economic analysis and is also of primary interest in psychology. However, the underlying mental processes and neuronal mechanisms are not well understood. Theories of human and animal choice have a cornerstone in the concept of 'value'. Consider, for example, a monkey offered one raisin versus one piece of apple: behavioural evidence suggests that the animal chooses by assigning values to the two options. But where and how values are represented in the brain is unclear. Here we show that, during economic choice, neurons in the orbitofrontal cortex (OFC) encode the value of offered and chosen goods. Notably, OFC neurons encode value independently of visuospatial factors and motor responses. If a monkey chooses between A and B, neurons in the OFC encode the value of the two goods independently of whether A is presented on the right and B on the left, or vice versa. This trait distinguishes the OFC from other brain areas in which value modulates activity related to sensory or motor processes. Our results have broad implications for possible psychological models, suggesting that economic choice is essentially choice between goods rather than choice between actions. In this framework, neurons in the OFC seem to be a good candidate network for value assignment underlying economic choice.
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                Author and article information

                Journal
                Neuron
                Neuron
                Elsevier BV
                08966273
                June 2016
                June 2016
                : 90
                : 6
                : 1299-1311
                Article
                10.1016/j.neuron.2016.04.045
                4911340
                27263972
                f6a1e6c2-e8fc-458a-8182-a191901c7b83
                © 2016
                History

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