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Role of medio-dorsal frontal and posterior parietal neurons during auditory detection performance in rats.

Bohon KS, Wiest MC - PLoS ONE (2014)

Bottom Line: To further characterize the role of frontal and parietal cortices in rat cognition, we recorded action potentials simultaneously from multiple sites in the medio-dorsal frontal cortex and posterior parietal cortex of rats while they performed a two-choice auditory detection task.We quantified neural correlates of task performance, including response movements, perception of a target tone, and the differentiation between stimuli with distinct features (different pitches or durations).In addition, we found a smaller and mostly not overlapping population of units that differentiated stimuli based on task-irrelevant details.

View Article: PubMed Central - PubMed

Affiliation: Wellesley College Neuroscience Program, Wellesley, Massachusetts, United States of America.

ABSTRACT
To further characterize the role of frontal and parietal cortices in rat cognition, we recorded action potentials simultaneously from multiple sites in the medio-dorsal frontal cortex and posterior parietal cortex of rats while they performed a two-choice auditory detection task. We quantified neural correlates of task performance, including response movements, perception of a target tone, and the differentiation between stimuli with distinct features (different pitches or durations). A minority of units--15% in frontal cortex, 23% in parietal cortex--significantly distinguished hit trials (successful detections, response movement to the right) from correct rejection trials (correct leftward response to the absence of the target tone). Estimating the contribution of movement-related activity to these responses suggested that more than half of these units were likely signaling correct perception of the auditory target, rather than merely movement direction. In addition, we found a smaller and mostly not overlapping population of units that differentiated stimuli based on task-irrelevant details. The detection-related spiking responses we observed suggest that correlates of perception in the rat are sparsely represented among neurons in the rat's frontal-parietal network, without being concentrated preferentially in frontal or parietal areas.

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Choice probability distributions from example trial-subsamples of all 217 frontal (left) and all 252 parietal (right) units of our reduced data set.The top panels show CP histograms with the whole population shown in white, candidate perceptual units (CPUs, which discriminate hits from CRs) shown in gray, and directional units (see below) shown in black. The CPUs that are not directional (visible gray part of bar) are considered to be putative perceptual units (PPUs, see text). The bottom panels show Hit-CR vs. miss-FA CP magnitude comparisons for the frontal (right) and parietal (left) units. Lines represent best linear fit of miss-FA and hit-CR differentiating units (black dots and line) and hit-CR only differentiating units (gray dots and line). Units with non-significant CPs are shown as unfilled circles. Those black dots which have consistent rate modulations for right vs. left movements across trial types (i.e. horizontal and vertical coordinates either both >0.5 or both <0.5) are considered “directional” units which could be primarily signaling movement-direction rather than perception of the target tone. Those units tend to lie along the y = x line, consistent with the expectation that CPs should be approximately equal for direction-related units for hits vs. CRs as for FAs vs. misses; whereas the CPUs that do not also discriminate FAs from misses do not lie near y = x, consistent with a role in perception.
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pone-0114064-g003: Choice probability distributions from example trial-subsamples of all 217 frontal (left) and all 252 parietal (right) units of our reduced data set.The top panels show CP histograms with the whole population shown in white, candidate perceptual units (CPUs, which discriminate hits from CRs) shown in gray, and directional units (see below) shown in black. The CPUs that are not directional (visible gray part of bar) are considered to be putative perceptual units (PPUs, see text). The bottom panels show Hit-CR vs. miss-FA CP magnitude comparisons for the frontal (right) and parietal (left) units. Lines represent best linear fit of miss-FA and hit-CR differentiating units (black dots and line) and hit-CR only differentiating units (gray dots and line). Units with non-significant CPs are shown as unfilled circles. Those black dots which have consistent rate modulations for right vs. left movements across trial types (i.e. horizontal and vertical coordinates either both >0.5 or both <0.5) are considered “directional” units which could be primarily signaling movement-direction rather than perception of the target tone. Those units tend to lie along the y = x line, consistent with the expectation that CPs should be approximately equal for direction-related units for hits vs. CRs as for FAs vs. misses; whereas the CPUs that do not also discriminate FAs from misses do not lie near y = x, consistent with a role in perception.

Mentions: To focus on potential perceptual responses to the target tone, we calculated choice probabilities based on the first second of spiking activity following the signal for signal trials, and the first second following the beep latency for that session on nonsignal trials. To identify candidate perception-related unit responses we initially calculated choice probabilities based on a comparison of hit trials versus correct rejections (CRs). Over all units and subsamples, the average hit-CR CP for both areas did not differ from chance, with a mean CP of 0.52 SE 0.01 in frontal units, and 0.49 SE 0.01 in parietal units. Nevertheless, we found a substantial fraction of units in each area whose firing in the second after the time of the target tone discriminated hits from CRs—we term these “candidate perception units” (CPUs; Figure 3 top panels). Averaged over the 20 subsamples (see Methods), 15 SE 1% of units [31/195] in frontal cortex and 23 SE 1% [80/349 units] in parietal cortex had hit-CR CPs significantly different from 0.5 (Figure 3 top panels, light gray). The trend towards a greater fraction of CPUs in parietal cortex is not quite significant (p = 0.051, chi-squared test). Now, on hits the rat correctly reported the presence of the target tone by moving to the right lickometer for water, whereas on CRs the rat correctly reported the absence of the target tone by moving to the left for water. Thus firing-rate differences between hits and CRs could be due to modulation of a unit by left vs. right movement, or due to the unit's involvement in perceiving the target tone.


Role of medio-dorsal frontal and posterior parietal neurons during auditory detection performance in rats.

Bohon KS, Wiest MC - PLoS ONE (2014)

Choice probability distributions from example trial-subsamples of all 217 frontal (left) and all 252 parietal (right) units of our reduced data set.The top panels show CP histograms with the whole population shown in white, candidate perceptual units (CPUs, which discriminate hits from CRs) shown in gray, and directional units (see below) shown in black. The CPUs that are not directional (visible gray part of bar) are considered to be putative perceptual units (PPUs, see text). The bottom panels show Hit-CR vs. miss-FA CP magnitude comparisons for the frontal (right) and parietal (left) units. Lines represent best linear fit of miss-FA and hit-CR differentiating units (black dots and line) and hit-CR only differentiating units (gray dots and line). Units with non-significant CPs are shown as unfilled circles. Those black dots which have consistent rate modulations for right vs. left movements across trial types (i.e. horizontal and vertical coordinates either both >0.5 or both <0.5) are considered “directional” units which could be primarily signaling movement-direction rather than perception of the target tone. Those units tend to lie along the y = x line, consistent with the expectation that CPs should be approximately equal for direction-related units for hits vs. CRs as for FAs vs. misses; whereas the CPUs that do not also discriminate FAs from misses do not lie near y = x, consistent with a role in perception.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4257565&req=5

pone-0114064-g003: Choice probability distributions from example trial-subsamples of all 217 frontal (left) and all 252 parietal (right) units of our reduced data set.The top panels show CP histograms with the whole population shown in white, candidate perceptual units (CPUs, which discriminate hits from CRs) shown in gray, and directional units (see below) shown in black. The CPUs that are not directional (visible gray part of bar) are considered to be putative perceptual units (PPUs, see text). The bottom panels show Hit-CR vs. miss-FA CP magnitude comparisons for the frontal (right) and parietal (left) units. Lines represent best linear fit of miss-FA and hit-CR differentiating units (black dots and line) and hit-CR only differentiating units (gray dots and line). Units with non-significant CPs are shown as unfilled circles. Those black dots which have consistent rate modulations for right vs. left movements across trial types (i.e. horizontal and vertical coordinates either both >0.5 or both <0.5) are considered “directional” units which could be primarily signaling movement-direction rather than perception of the target tone. Those units tend to lie along the y = x line, consistent with the expectation that CPs should be approximately equal for direction-related units for hits vs. CRs as for FAs vs. misses; whereas the CPUs that do not also discriminate FAs from misses do not lie near y = x, consistent with a role in perception.
Mentions: To focus on potential perceptual responses to the target tone, we calculated choice probabilities based on the first second of spiking activity following the signal for signal trials, and the first second following the beep latency for that session on nonsignal trials. To identify candidate perception-related unit responses we initially calculated choice probabilities based on a comparison of hit trials versus correct rejections (CRs). Over all units and subsamples, the average hit-CR CP for both areas did not differ from chance, with a mean CP of 0.52 SE 0.01 in frontal units, and 0.49 SE 0.01 in parietal units. Nevertheless, we found a substantial fraction of units in each area whose firing in the second after the time of the target tone discriminated hits from CRs—we term these “candidate perception units” (CPUs; Figure 3 top panels). Averaged over the 20 subsamples (see Methods), 15 SE 1% of units [31/195] in frontal cortex and 23 SE 1% [80/349 units] in parietal cortex had hit-CR CPs significantly different from 0.5 (Figure 3 top panels, light gray). The trend towards a greater fraction of CPUs in parietal cortex is not quite significant (p = 0.051, chi-squared test). Now, on hits the rat correctly reported the presence of the target tone by moving to the right lickometer for water, whereas on CRs the rat correctly reported the absence of the target tone by moving to the left for water. Thus firing-rate differences between hits and CRs could be due to modulation of a unit by left vs. right movement, or due to the unit's involvement in perceiving the target tone.

Bottom Line: To further characterize the role of frontal and parietal cortices in rat cognition, we recorded action potentials simultaneously from multiple sites in the medio-dorsal frontal cortex and posterior parietal cortex of rats while they performed a two-choice auditory detection task.We quantified neural correlates of task performance, including response movements, perception of a target tone, and the differentiation between stimuli with distinct features (different pitches or durations).In addition, we found a smaller and mostly not overlapping population of units that differentiated stimuli based on task-irrelevant details.

View Article: PubMed Central - PubMed

Affiliation: Wellesley College Neuroscience Program, Wellesley, Massachusetts, United States of America.

ABSTRACT
To further characterize the role of frontal and parietal cortices in rat cognition, we recorded action potentials simultaneously from multiple sites in the medio-dorsal frontal cortex and posterior parietal cortex of rats while they performed a two-choice auditory detection task. We quantified neural correlates of task performance, including response movements, perception of a target tone, and the differentiation between stimuli with distinct features (different pitches or durations). A minority of units--15% in frontal cortex, 23% in parietal cortex--significantly distinguished hit trials (successful detections, response movement to the right) from correct rejection trials (correct leftward response to the absence of the target tone). Estimating the contribution of movement-related activity to these responses suggested that more than half of these units were likely signaling correct perception of the auditory target, rather than merely movement direction. In addition, we found a smaller and mostly not overlapping population of units that differentiated stimuli based on task-irrelevant details. The detection-related spiking responses we observed suggest that correlates of perception in the rat are sparsely represented among neurons in the rat's frontal-parietal network, without being concentrated preferentially in frontal or parietal areas.

Show MeSH
Related in: MedlinePlus