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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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Choice-selective neurons in PPC and FOF exhibit signatures of evidence accumulationa, Sequence of events for each trial. b, Schematic of the evidence accumulation process. Each right (left) click provides a single quantum of positive (negative) evidence. The thick green line shows the expected trajectory, averaged over many trials, of the accumulating evidence for a mean stimulus strength of 29:11 clicks/sec. The red line shows this for 15:25 clicks/sec. The lighter-colored traces show how individual trials within a given stimulus-difficulty class meander based on each trial’s variable click times. At the “go” signal (offset of center LED), the sign of a indicates the appropriate decision. c, PPC population responses. Trials were grouped by average strength of the sensory evidence. Green traces correspond to stimuli in the preferred direction of the recorded neurons and red traces to the non-preferred direction. Darker hues correspond to easier trials. Responses exhibit ramping profiles that depend on the mean stimulus strength. The PPC response lag (RL) until stimulus-strength-dependent ramping was ≈200 ms. n = 93 neurons. d, Same as (c) for neurons in the FOF. Similar to PPC, responses exhibit ramping profiles that depend on the mean stimulus strength. RL in the FOF is ≈100 ms. n = 128 neurons. e, Click-triggered average response ± s.e.m. in PPC. f, Same as (e) for FOF.
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Figure 1: Choice-selective neurons in PPC and FOF exhibit signatures of evidence accumulationa, Sequence of events for each trial. b, Schematic of the evidence accumulation process. Each right (left) click provides a single quantum of positive (negative) evidence. The thick green line shows the expected trajectory, averaged over many trials, of the accumulating evidence for a mean stimulus strength of 29:11 clicks/sec. The red line shows this for 15:25 clicks/sec. The lighter-colored traces show how individual trials within a given stimulus-difficulty class meander based on each trial’s variable click times. At the “go” signal (offset of center LED), the sign of a indicates the appropriate decision. c, PPC population responses. Trials were grouped by average strength of the sensory evidence. Green traces correspond to stimuli in the preferred direction of the recorded neurons and red traces to the non-preferred direction. Darker hues correspond to easier trials. Responses exhibit ramping profiles that depend on the mean stimulus strength. The PPC response lag (RL) until stimulus-strength-dependent ramping was ≈200 ms. n = 93 neurons. d, Same as (c) for neurons in the FOF. Similar to PPC, responses exhibit ramping profiles that depend on the mean stimulus strength. RL in the FOF is ≈100 ms. n = 128 neurons. e, Click-triggered average response ± s.e.m. in PPC. f, Same as (e) for FOF.

Mentions: We trained rats on a previously developed decision task in which subjects accumulate sensory evidence over many hundreds of milliseconds to inform a binary left-right choice (“Poisson Clicks” task, Fig. 1a, Extended Data Fig. 1a–c)10. On each trial, rats kept their nose in a central port during the presentation of two simultaneous trains of randomly-timed auditory clicks, one played from a speaker to their left and the other from a speaker to their right. At the end of the variable-duration stimulus, the rat’s task was to decide which side had played the greater total number of clicks (Fig. 1a). Easy trials had a large mean rate difference between the two click trains (e.g., 39:1 clicks/sec), while difficult trials had a small mean rate difference (e.g., 21:19 clicks/sec). Accumulation of evidence models predict that averaging within a given difficulty class will produce a mean trajectory for the accumulated evidence that gradually ramps over time with a slope proportional to the mean strength of the sensory evidence (Fig. 1b). This type of correlate of evidence accumulation has been reported in several interconnected primate brain regions, including the PPC and frontal eye fields3–5,7,8,11. To examine whether signatures of evidence accumulation are present in the rodent brain, we recorded from 394 neurons in PPC of 4 rats and 397 neurons in FOF of 6 rats while they performed the Poisson Clicks task. These two areas that have been suggested as potential rat homologues of primate PPC and FEF12,13. We recorded all isolatable neurons encountered regardless of response properties. Ninety-three neurons in PPC (23%) and 128 neurons in FOF (32%) exhibited firing rates during the pre-movement period (from stimulus onset to center port withdrawal) that were significantly different (p<0.05) for trials that subsequently ended with a right versus a left choice. This pre-movement side selectivity is consistent with previous findings in both rat PPC14,15 and FOF13. We focus on these pre-movement side-selective neurons because they are most likely to play a role in decision formation.


Distinct relationships of parietal and prefrontal cortices to evidence accumulation.

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

Choice-selective neurons in PPC and FOF exhibit signatures of evidence accumulationa, Sequence of events for each trial. b, Schematic of the evidence accumulation process. Each right (left) click provides a single quantum of positive (negative) evidence. The thick green line shows the expected trajectory, averaged over many trials, of the accumulating evidence for a mean stimulus strength of 29:11 clicks/sec. The red line shows this for 15:25 clicks/sec. The lighter-colored traces show how individual trials within a given stimulus-difficulty class meander based on each trial’s variable click times. At the “go” signal (offset of center LED), the sign of a indicates the appropriate decision. c, PPC population responses. Trials were grouped by average strength of the sensory evidence. Green traces correspond to stimuli in the preferred direction of the recorded neurons and red traces to the non-preferred direction. Darker hues correspond to easier trials. Responses exhibit ramping profiles that depend on the mean stimulus strength. The PPC response lag (RL) until stimulus-strength-dependent ramping was ≈200 ms. n = 93 neurons. d, Same as (c) for neurons in the FOF. Similar to PPC, responses exhibit ramping profiles that depend on the mean stimulus strength. RL in the FOF is ≈100 ms. n = 128 neurons. e, Click-triggered average response ± s.e.m. in PPC. f, Same as (e) for FOF.
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Figure 1: Choice-selective neurons in PPC and FOF exhibit signatures of evidence accumulationa, Sequence of events for each trial. b, Schematic of the evidence accumulation process. Each right (left) click provides a single quantum of positive (negative) evidence. The thick green line shows the expected trajectory, averaged over many trials, of the accumulating evidence for a mean stimulus strength of 29:11 clicks/sec. The red line shows this for 15:25 clicks/sec. The lighter-colored traces show how individual trials within a given stimulus-difficulty class meander based on each trial’s variable click times. At the “go” signal (offset of center LED), the sign of a indicates the appropriate decision. c, PPC population responses. Trials were grouped by average strength of the sensory evidence. Green traces correspond to stimuli in the preferred direction of the recorded neurons and red traces to the non-preferred direction. Darker hues correspond to easier trials. Responses exhibit ramping profiles that depend on the mean stimulus strength. The PPC response lag (RL) until stimulus-strength-dependent ramping was ≈200 ms. n = 93 neurons. d, Same as (c) for neurons in the FOF. Similar to PPC, responses exhibit ramping profiles that depend on the mean stimulus strength. RL in the FOF is ≈100 ms. n = 128 neurons. e, Click-triggered average response ± s.e.m. in PPC. f, Same as (e) for FOF.
Mentions: We trained rats on a previously developed decision task in which subjects accumulate sensory evidence over many hundreds of milliseconds to inform a binary left-right choice (“Poisson Clicks” task, Fig. 1a, Extended Data Fig. 1a–c)10. On each trial, rats kept their nose in a central port during the presentation of two simultaneous trains of randomly-timed auditory clicks, one played from a speaker to their left and the other from a speaker to their right. At the end of the variable-duration stimulus, the rat’s task was to decide which side had played the greater total number of clicks (Fig. 1a). Easy trials had a large mean rate difference between the two click trains (e.g., 39:1 clicks/sec), while difficult trials had a small mean rate difference (e.g., 21:19 clicks/sec). Accumulation of evidence models predict that averaging within a given difficulty class will produce a mean trajectory for the accumulated evidence that gradually ramps over time with a slope proportional to the mean strength of the sensory evidence (Fig. 1b). This type of correlate of evidence accumulation has been reported in several interconnected primate brain regions, including the PPC and frontal eye fields3–5,7,8,11. To examine whether signatures of evidence accumulation are present in the rodent brain, we recorded from 394 neurons in PPC of 4 rats and 397 neurons in FOF of 6 rats while they performed the Poisson Clicks task. These two areas that have been suggested as potential rat homologues of primate PPC and FEF12,13. We recorded all isolatable neurons encountered regardless of response properties. Ninety-three neurons in PPC (23%) and 128 neurons in FOF (32%) exhibited firing rates during the pre-movement period (from stimulus onset to center port withdrawal) that were significantly different (p<0.05) for trials that subsequently ended with a right versus a left choice. This pre-movement side selectivity is consistent with previous findings in both rat PPC14,15 and FOF13. We focus on these pre-movement side-selective neurons because they are most likely to play a role in decision formation.

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