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Distinct relationships of parietal and prefrontal cortices to evidence accumulation.

Hanks TD, Kopec CD, Brunton BW, Duan CA, Erlich JC, Brody CD - Nature (2015)

Bottom Line: Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions.Classical analyses uncovered correlates of accumulating evidence, similar to previous observations in primates and also similar across the two regions.Our results place important constraints on the circuit logic of brain regions involved in decision-making.

View Article: PubMed Central - PubMed

Affiliation: 1] Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA [2] Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.

ABSTRACT
Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions. Here we develop a generalizable method to measure tuning curves that specify the relationship between neural responses and mentally accumulated evidence, and apply it to distinguish the encoding of decision variables in posterior parietal cortex and prefrontal cortex (frontal orienting fields, FOF). We recorded the firing rates of neurons in posterior parietal cortex and FOF from rats performing a perceptual decision-making task. Classical analyses uncovered correlates of accumulating evidence, similar to previous observations in primates and also similar across the two regions. However, tuning curve assays revealed that while the posterior parietal cortex encodes a graded value of the accumulating evidence, the FOF has a more categorical encoding that indicates, throughout the trial, the decision provisionally favoured by the evidence accumulated so far. Contrary to current views, this suggests that premotor activity in the frontal cortex does not have a role in the accumulation process, but instead has a more categorical function, such as transforming accumulated evidence into a discrete choice. To probe causally the role of FOF activity, we optogenetically silenced it during different time points of the trial. Consistent with a role in committing to a categorical choice at the end of the evidence accumulation process, but not consistent with a role during the accumulation itself, a behavioural effect was observed only when FOF silencing occurred at the end of the perceptual stimulus. Our results place important constraints on the circuit logic of brain regions involved in decision-making.

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PPC encodes graded accumulated evidence while FOF has a more categorical encodinga, Relationship between PPC population firing rate and accumulator value aligned to the stimulus onset minus the neural response lag (200 ms for PPC). Colors indicate accumulator value with ±B corresponding to sticky accumulation bounds. The a → r map in PPC is graded and relatively stable over time. n = 93 neurons. b, Same as (a) for FOF (100 ms neural response lag). The a → r map is again relatively stable over time, but the responses appear to be more clustered based on the sign of a. n = 128 neurons. c, Average ± s.e.m. over the full time period shown (t=0.15 to t=0.5). PPC, in black; FOF, in red. Responses were scaled to span the range from 0 to 1 to account for differences in dynamic range. PPC shows a smoothly graded relationship, while FOF shows a sharper dependence on the sign of the accumulator value. d, Relationship between PPC population and accumulator value aligned to the putative end of the decision process, which is defined as the time relative to the stimulus end minus the response lag.
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Figure 3: PPC encodes graded accumulated evidence while FOF has a more categorical encodinga, Relationship between PPC population firing rate and accumulator value aligned to the stimulus onset minus the neural response lag (200 ms for PPC). Colors indicate accumulator value with ±B corresponding to sticky accumulation bounds. The a → r map in PPC is graded and relatively stable over time. n = 93 neurons. b, Same as (a) for FOF (100 ms neural response lag). The a → r map is again relatively stable over time, but the responses appear to be more clustered based on the sign of a. n = 128 neurons. c, Average ± s.e.m. over the full time period shown (t=0.15 to t=0.5). PPC, in black; FOF, in red. Responses were scaled to span the range from 0 to 1 to account for differences in dynamic range. PPC shows a smoothly graded relationship, while FOF shows a sharper dependence on the sign of the accumulator value. d, Relationship between PPC population and accumulator value aligned to the putative end of the decision process, which is defined as the time relative to the stimulus end minus the response lag.

Mentions: This analysis revealed that PPC encoded the accumulator’s evolving value a(t) using a graded map that is stable across time (Fig. 3a). A similar encoding was observed in monkey PPC, albeit using a task that did not require a temporal accumulation strategy17. Thus, during decision formation, firing rates in PPC change over time as the accumulated evidence changes, but at any timepoint the graded value of the accumulator is encoded, by a fixed map, into a graded firing rate. In this way, the firing rate provides the answer to the question “what is the value of the mentally accumulated evidence?”


Distinct relationships of parietal and prefrontal cortices to evidence accumulation.

Hanks TD, Kopec CD, Brunton BW, Duan CA, Erlich JC, Brody CD - Nature (2015)

PPC encodes graded accumulated evidence while FOF has a more categorical encodinga, Relationship between PPC population firing rate and accumulator value aligned to the stimulus onset minus the neural response lag (200 ms for PPC). Colors indicate accumulator value with ±B corresponding to sticky accumulation bounds. The a → r map in PPC is graded and relatively stable over time. n = 93 neurons. b, Same as (a) for FOF (100 ms neural response lag). The a → r map is again relatively stable over time, but the responses appear to be more clustered based on the sign of a. n = 128 neurons. c, Average ± s.e.m. over the full time period shown (t=0.15 to t=0.5). PPC, in black; FOF, in red. Responses were scaled to span the range from 0 to 1 to account for differences in dynamic range. PPC shows a smoothly graded relationship, while FOF shows a sharper dependence on the sign of the accumulator value. d, Relationship between PPC population and accumulator value aligned to the putative end of the decision process, which is defined as the time relative to the stimulus end minus the response lag.
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Related In: Results  -  Collection

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Figure 3: PPC encodes graded accumulated evidence while FOF has a more categorical encodinga, Relationship between PPC population firing rate and accumulator value aligned to the stimulus onset minus the neural response lag (200 ms for PPC). Colors indicate accumulator value with ±B corresponding to sticky accumulation bounds. The a → r map in PPC is graded and relatively stable over time. n = 93 neurons. b, Same as (a) for FOF (100 ms neural response lag). The a → r map is again relatively stable over time, but the responses appear to be more clustered based on the sign of a. n = 128 neurons. c, Average ± s.e.m. over the full time period shown (t=0.15 to t=0.5). PPC, in black; FOF, in red. Responses were scaled to span the range from 0 to 1 to account for differences in dynamic range. PPC shows a smoothly graded relationship, while FOF shows a sharper dependence on the sign of the accumulator value. d, Relationship between PPC population and accumulator value aligned to the putative end of the decision process, which is defined as the time relative to the stimulus end minus the response lag.
Mentions: This analysis revealed that PPC encoded the accumulator’s evolving value a(t) using a graded map that is stable across time (Fig. 3a). A similar encoding was observed in monkey PPC, albeit using a task that did not require a temporal accumulation strategy17. Thus, during decision formation, firing rates in PPC change over time as the accumulated evidence changes, but at any timepoint the graded value of the accumulator is encoded, by a fixed map, into a graded firing rate. In this way, the firing rate provides the answer to the question “what is the value of the mentally accumulated evidence?”

Bottom Line: Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions.Classical analyses uncovered correlates of accumulating evidence, similar to previous observations in primates and also similar across the two regions.Our results place important constraints on the circuit logic of brain regions involved in decision-making.

View Article: PubMed Central - PubMed

Affiliation: 1] Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA [2] Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA.

ABSTRACT
Gradual accumulation of evidence is thought to be fundamental for decision-making, and its neural correlates have been found in several brain regions. Here we develop a generalizable method to measure tuning curves that specify the relationship between neural responses and mentally accumulated evidence, and apply it to distinguish the encoding of decision variables in posterior parietal cortex and prefrontal cortex (frontal orienting fields, FOF). We recorded the firing rates of neurons in posterior parietal cortex and FOF from rats performing a perceptual decision-making task. Classical analyses uncovered correlates of accumulating evidence, similar to previous observations in primates and also similar across the two regions. However, tuning curve assays revealed that while the posterior parietal cortex encodes a graded value of the accumulating evidence, the FOF has a more categorical encoding that indicates, throughout the trial, the decision provisionally favoured by the evidence accumulated so far. Contrary to current views, this suggests that premotor activity in the frontal cortex does not have a role in the accumulation process, but instead has a more categorical function, such as transforming accumulated evidence into a discrete choice. To probe causally the role of FOF activity, we optogenetically silenced it during different time points of the trial. Consistent with a role in committing to a categorical choice at the end of the evidence accumulation process, but not consistent with a role during the accumulation itself, a behavioural effect was observed only when FOF silencing occurred at the end of the perceptual stimulus. Our results place important constraints on the circuit logic of brain regions involved in decision-making.

Show MeSH
Related in: MedlinePlus