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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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Temporally-precise transient halorhodopsin-mediated inactivation reveals that FOF activity has a significant impact on decision formation only at the end of the auditory stimulus presentationa, b, c, The task structure is shown at the top. For the lower panels, the horizontal extent of the thick black or colored bars indicates the period of inactivation (laser on). The vertical position indicates the average bias across rats induced by the corresponding period of FOF inactivation (% “went ipsi” laser on - “went ipsi” laser off). Asterisks indicate p<0.01 (bootstrap) of effect size or comparison. a, Bias caused by “full-trial” (2 s long laser pulse) inactivation. n = 18 rats. b, Bias caused by 500 ms inactivation during the pre-stimulus period (red; n = 5 rats), the first half of the stimulus (yellow; n = 9), the second half of the stimulus (“peri-choice”, green; n = 9), or the post-stimulus movement (purple; n = 5). c, Bias caused by 250 ms inactivation during the next-to-last 250 ms (light blue; n = 7), or the final 250 ms (“peri-choice”, magenta; n = 7) of a 0.6 to 1.0 s duration stimulus. d, Peri-choice inactivation bias normalized by “full-trial” inactivation bias (500 ms group in green; 250 ms, in magenta). Normalization performed for each rat independently. For all panels, error bars show s.e.m. across rats.
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Figure 4: Temporally-precise transient halorhodopsin-mediated inactivation reveals that FOF activity has a significant impact on decision formation only at the end of the auditory stimulus presentationa, b, c, The task structure is shown at the top. For the lower panels, the horizontal extent of the thick black or colored bars indicates the period of inactivation (laser on). The vertical position indicates the average bias across rats induced by the corresponding period of FOF inactivation (% “went ipsi” laser on - “went ipsi” laser off). Asterisks indicate p<0.01 (bootstrap) of effect size or comparison. a, Bias caused by “full-trial” (2 s long laser pulse) inactivation. n = 18 rats. b, Bias caused by 500 ms inactivation during the pre-stimulus period (red; n = 5 rats), the first half of the stimulus (yellow; n = 9), the second half of the stimulus (“peri-choice”, green; n = 9), or the post-stimulus movement (purple; n = 5). c, Bias caused by 250 ms inactivation during the next-to-last 250 ms (light blue; n = 7), or the final 250 ms (“peri-choice”, magenta; n = 7) of a 0.6 to 1.0 s duration stimulus. d, Peri-choice inactivation bias normalized by “full-trial” inactivation bias (500 ms group in green; 250 ms, in magenta). Normalization performed for each rat independently. For all panels, error bars show s.e.m. across rats.

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)

Temporally-precise transient halorhodopsin-mediated inactivation reveals that FOF activity has a significant impact on decision formation only at the end of the auditory stimulus presentationa, b, c, The task structure is shown at the top. For the lower panels, the horizontal extent of the thick black or colored bars indicates the period of inactivation (laser on). The vertical position indicates the average bias across rats induced by the corresponding period of FOF inactivation (% “went ipsi” laser on - “went ipsi” laser off). Asterisks indicate p<0.01 (bootstrap) of effect size or comparison. a, Bias caused by “full-trial” (2 s long laser pulse) inactivation. n = 18 rats. b, Bias caused by 500 ms inactivation during the pre-stimulus period (red; n = 5 rats), the first half of the stimulus (yellow; n = 9), the second half of the stimulus (“peri-choice”, green; n = 9), or the post-stimulus movement (purple; n = 5). c, Bias caused by 250 ms inactivation during the next-to-last 250 ms (light blue; n = 7), or the final 250 ms (“peri-choice”, magenta; n = 7) of a 0.6 to 1.0 s duration stimulus. d, Peri-choice inactivation bias normalized by “full-trial” inactivation bias (500 ms group in green; 250 ms, in magenta). Normalization performed for each rat independently. For all panels, error bars show s.e.m. across rats.
© Copyright Policy - permissions-link
Related In: Results  -  Collection

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Figure 4: Temporally-precise transient halorhodopsin-mediated inactivation reveals that FOF activity has a significant impact on decision formation only at the end of the auditory stimulus presentationa, b, c, The task structure is shown at the top. For the lower panels, the horizontal extent of the thick black or colored bars indicates the period of inactivation (laser on). The vertical position indicates the average bias across rats induced by the corresponding period of FOF inactivation (% “went ipsi” laser on - “went ipsi” laser off). Asterisks indicate p<0.01 (bootstrap) of effect size or comparison. a, Bias caused by “full-trial” (2 s long laser pulse) inactivation. n = 18 rats. b, Bias caused by 500 ms inactivation during the pre-stimulus period (red; n = 5 rats), the first half of the stimulus (yellow; n = 9), the second half of the stimulus (“peri-choice”, green; n = 9), or the post-stimulus movement (purple; n = 5). c, Bias caused by 250 ms inactivation during the next-to-last 250 ms (light blue; n = 7), or the final 250 ms (“peri-choice”, magenta; n = 7) of a 0.6 to 1.0 s duration stimulus. d, Peri-choice inactivation bias normalized by “full-trial” inactivation bias (500 ms group in green; 250 ms, in magenta). Normalization performed for each rat independently. For all panels, error bars show s.e.m. across rats.
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