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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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Model-based analysis of halorhodopsin mediated inactivation of the FOF, following Erlich et al. (submitted)a–f, Full-trial inactivation (figure 4a of main text). a, Control trials with no inactivation taken from sessions with full-trial, 2 s, halorhodopsin inactivation. “Contra” and “Ipsi” sides are relative to the side of the FOF that was inactivated on non-control trials. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. b, Comparison of the negative log likelihood for each candidate source of bias (see Methods). Smaller values correspond to a better fit. The post-categorization bias was significantly better than all other alternatives (p < 0.05, bootstrap). c–f, Data points show the proportion of contralateral choices for full-trial, 2 s inactivation of FOF. The curves show choice behavior predicted by each alternative implementation of choice bias. b, Post-categorization bias. c, Accumulator shift. d, Unbalanced input gain. e, Unbalanced input noise. g–j, Peri-choice inactivation (figure 4b–d of main text). g, Control trials with no inactivation taken from sessions with either 500 ms or 250 ms peri-choice inactivation. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. h, Comparison of the negative log likelihood for both sources of bias. Smaller values correspond to a better fit. The post-categorization bias was significantly better than the accumulator bias (p < 0.05, bootstrap). i–j, Data points show the proportion of contralateral choices for peri-choice inactivation of FOF. The curves show choice behavior predicted by the two versions of bias that predict an effect only at the end of the stimulus period. i, Post-categorization bias. j, Accumulator shift.
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Figure 12: Model-based analysis of halorhodopsin mediated inactivation of the FOF, following Erlich et al. (submitted)a–f, Full-trial inactivation (figure 4a of main text). a, Control trials with no inactivation taken from sessions with full-trial, 2 s, halorhodopsin inactivation. “Contra” and “Ipsi” sides are relative to the side of the FOF that was inactivated on non-control trials. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. b, Comparison of the negative log likelihood for each candidate source of bias (see Methods). Smaller values correspond to a better fit. The post-categorization bias was significantly better than all other alternatives (p < 0.05, bootstrap). c–f, Data points show the proportion of contralateral choices for full-trial, 2 s inactivation of FOF. The curves show choice behavior predicted by each alternative implementation of choice bias. b, Post-categorization bias. c, Accumulator shift. d, Unbalanced input gain. e, Unbalanced input noise. g–j, Peri-choice inactivation (figure 4b–d of main text). g, Control trials with no inactivation taken from sessions with either 500 ms or 250 ms peri-choice inactivation. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. h, Comparison of the negative log likelihood for both sources of bias. Smaller values correspond to a better fit. The post-categorization bias was significantly better than the accumulator bias (p < 0.05, bootstrap). i–j, Data points show the proportion of contralateral choices for peri-choice inactivation of FOF. The curves show choice behavior predicted by the two versions of bias that predict an effect only at the end of the stimulus period. i, Post-categorization bias. j, Accumulator shift.

Mentions: To test these predictions, we used halorhodopsin eNpHR3.0 to unilaterally and transiently inactivate the FOF during the Poisson Clicks task (Extended Data Fig. 7). Full-trial inactivation (2 s period from 500 ms before auditory stimulus onset until 500 ms after stimulus end, Fig. 4a) resulted in a significant ipsilateral choice bias (10.3 ± 3.0%, p<0.01, mean ± SEM across rats). We next assessed the temporal specificity of the effect of FOF inactivation using four different 500-ms time periods: the delay before stimulus onset, the first half of a 1-sec stimulus, the second half of a 1-sec stimulus (“peri-choice”), or the movement period (“post-choice”). Only peri-choice inactivation led to a significant ipsilateral bias (Fig. 4b, 10.6 ± 1.0%, p<0.01). Inactivation during the early accumulation period produced a smaller effect (p<0.01) that was not significantly different from zero (p=0.48). In a second group of rats we used even shorter inactivation periods: either the next-to-last, or the final (“peri-choice”) 250 ms of a variable-duration click train. Again, only the peri-choice perturbation had an effect on behavior (Fig. 4c, 5.4 ± 0.8%, p<0.01), while the effect of perturbation just 250 ms earlier was smaller than the peri-choice effect (p<0.01) and not statistically significant (p=0.45). Furthermore, in both the 500-ms and 250-ms groups of rats, the magnitude of the bias induced by peri-choice inactivation fully explained the magnitude of the bias for full-trial inactivation (Fig. 4d, peri-choice normalized by full-trial bias = 1.17 ± 0.45 and 0.93 ± 0.33 for each group, respectively). Consistent with the idea that the FOF’s dominant role is to control the categorical choice, a model-based analysis indicated that a post-categorization bias explained these optogenetic inactivation data significantly better than alternative forms of bias that directly affected the accumulation process18 (p < 0.05, see Methods; Extended Data Fig. 8). Finally, and again consistent with the FOF playing a role that is separate from the click accumulation process, we found no correlation between choice biases induced by unilateral perturbation and click counts or stimulus duration (Extended Data Fig. 9).


Distinct relationships of parietal and prefrontal cortices to evidence accumulation.

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

Model-based analysis of halorhodopsin mediated inactivation of the FOF, following Erlich et al. (submitted)a–f, Full-trial inactivation (figure 4a of main text). a, Control trials with no inactivation taken from sessions with full-trial, 2 s, halorhodopsin inactivation. “Contra” and “Ipsi” sides are relative to the side of the FOF that was inactivated on non-control trials. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. b, Comparison of the negative log likelihood for each candidate source of bias (see Methods). Smaller values correspond to a better fit. The post-categorization bias was significantly better than all other alternatives (p < 0.05, bootstrap). c–f, Data points show the proportion of contralateral choices for full-trial, 2 s inactivation of FOF. The curves show choice behavior predicted by each alternative implementation of choice bias. b, Post-categorization bias. c, Accumulator shift. d, Unbalanced input gain. e, Unbalanced input noise. g–j, Peri-choice inactivation (figure 4b–d of main text). g, Control trials with no inactivation taken from sessions with either 500 ms or 250 ms peri-choice inactivation. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. h, Comparison of the negative log likelihood for both sources of bias. Smaller values correspond to a better fit. The post-categorization bias was significantly better than the accumulator bias (p < 0.05, bootstrap). i–j, Data points show the proportion of contralateral choices for peri-choice inactivation of FOF. The curves show choice behavior predicted by the two versions of bias that predict an effect only at the end of the stimulus period. i, Post-categorization bias. j, Accumulator shift.
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Related In: Results  -  Collection

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Figure 12: Model-based analysis of halorhodopsin mediated inactivation of the FOF, following Erlich et al. (submitted)a–f, Full-trial inactivation (figure 4a of main text). a, Control trials with no inactivation taken from sessions with full-trial, 2 s, halorhodopsin inactivation. “Contra” and “Ipsi” sides are relative to the side of the FOF that was inactivated on non-control trials. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. b, Comparison of the negative log likelihood for each candidate source of bias (see Methods). Smaller values correspond to a better fit. The post-categorization bias was significantly better than all other alternatives (p < 0.05, bootstrap). c–f, Data points show the proportion of contralateral choices for full-trial, 2 s inactivation of FOF. The curves show choice behavior predicted by each alternative implementation of choice bias. b, Post-categorization bias. c, Accumulator shift. d, Unbalanced input gain. e, Unbalanced input noise. g–j, Peri-choice inactivation (figure 4b–d of main text). g, Control trials with no inactivation taken from sessions with either 500 ms or 250 ms peri-choice inactivation. The curve shows the psychometric function predicted by the best-fit behavioral model based on the same stimuli that produced the behavior. h, Comparison of the negative log likelihood for both sources of bias. Smaller values correspond to a better fit. The post-categorization bias was significantly better than the accumulator bias (p < 0.05, bootstrap). i–j, Data points show the proportion of contralateral choices for peri-choice inactivation of FOF. The curves show choice behavior predicted by the two versions of bias that predict an effect only at the end of the stimulus period. i, Post-categorization bias. j, Accumulator shift.
Mentions: To test these predictions, we used halorhodopsin eNpHR3.0 to unilaterally and transiently inactivate the FOF during the Poisson Clicks task (Extended Data Fig. 7). Full-trial inactivation (2 s period from 500 ms before auditory stimulus onset until 500 ms after stimulus end, Fig. 4a) resulted in a significant ipsilateral choice bias (10.3 ± 3.0%, p<0.01, mean ± SEM across rats). We next assessed the temporal specificity of the effect of FOF inactivation using four different 500-ms time periods: the delay before stimulus onset, the first half of a 1-sec stimulus, the second half of a 1-sec stimulus (“peri-choice”), or the movement period (“post-choice”). Only peri-choice inactivation led to a significant ipsilateral bias (Fig. 4b, 10.6 ± 1.0%, p<0.01). Inactivation during the early accumulation period produced a smaller effect (p<0.01) that was not significantly different from zero (p=0.48). In a second group of rats we used even shorter inactivation periods: either the next-to-last, or the final (“peri-choice”) 250 ms of a variable-duration click train. Again, only the peri-choice perturbation had an effect on behavior (Fig. 4c, 5.4 ± 0.8%, p<0.01), while the effect of perturbation just 250 ms earlier was smaller than the peri-choice effect (p<0.01) and not statistically significant (p=0.45). Furthermore, in both the 500-ms and 250-ms groups of rats, the magnitude of the bias induced by peri-choice inactivation fully explained the magnitude of the bias for full-trial inactivation (Fig. 4d, peri-choice normalized by full-trial bias = 1.17 ± 0.45 and 0.93 ± 0.33 for each group, respectively). Consistent with the idea that the FOF’s dominant role is to control the categorical choice, a model-based analysis indicated that a post-categorization bias explained these optogenetic inactivation data significantly better than alternative forms of bias that directly affected the accumulation process18 (p < 0.05, see Methods; Extended Data Fig. 8). Finally, and again consistent with the FOF playing a role that is separate from the click accumulation process, we found no correlation between choice biases induced by unilateral perturbation and click counts or stimulus duration (Extended Data Fig. 9).

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