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Rapid learning in visual cortical networks.

Wang Y, Dragoi V - Elife (2015)

Bottom Line: We show that the increase in behavioral performance during learning is predicted by a tight coordination of spike timing with local population activity.More spike-LFP theta synchronization is correlated with higher learning performance, while high-frequency synchronization is unrelated with changes in performance, but these changes were absent once learning had stabilized and stimuli became familiar, or in the absence of learning.These findings reveal a novel mechanism of plasticity in visual cortex by which elevated low-frequency synchronization between individual neurons and local population activity accompanies the improvement in performance during learning.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston, Houston, United States.

ABSTRACT
Although changes in brain activity during learning have been extensively examined at the single neuron level, the coding strategies employed by cell populations remain mysterious. We examined cell populations in macaque area V4 during a rapid form of perceptual learning that emerges within tens of minutes. Multiple single units and LFP responses were recorded as monkeys improved their performance in an image discrimination task. We show that the increase in behavioral performance during learning is predicted by a tight coordination of spike timing with local population activity. More spike-LFP theta synchronization is correlated with higher learning performance, while high-frequency synchronization is unrelated with changes in performance, but these changes were absent once learning had stabilized and stimuli became familiar, or in the absence of learning. These findings reveal a novel mechanism of plasticity in visual cortex by which elevated low-frequency synchronization between individual neurons and local population activity accompanies the improvement in performance during learning.

No MeSH data available.


Related in: MedlinePlus

Control experiment—(A) Monkey 2 performed control experiments (n = 12 sessions, 741 cell pairs) in which novel natural scenes were flashed in the neurons' receptive fields, while the animal was engaged in a red/green color detection task in the contralateral hemifield.Briefly, after 500 ms of fixation, a 5-deg natural scene and a red square (3 deg in diameter) were presented simultaneously for the same random duration (1000–1800 ms) at two symmetric locations on the screen. The animal was required to signal the color change for the attended square (from red to green) within the next 3000 ms. Each session consisted of 400 trials. (B) We examined the block-by-block (each block consisted of 100 trials) changes in spike-LFP coherence (SFC) when the image was presented in the neurons' receptive fields (during the first 1000-ms of stimulus presentation). The results (shown as SFC changes with respect to SFC in block 1) confirm the results of our first control experiment (Figure 6A), that is, we were unable to detect significant block-by-block changes in SFC in any frequency band during inattentive (passive) fixation (theta: p = 0.99, alpha: p = 0.21, beta: p = 0.25, gamma: p = 0.49, Kruskal–Wallis test).DOI:http://dx.doi.org/10.7554/eLife.08417.010
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fig6s1: Control experiment—(A) Monkey 2 performed control experiments (n = 12 sessions, 741 cell pairs) in which novel natural scenes were flashed in the neurons' receptive fields, while the animal was engaged in a red/green color detection task in the contralateral hemifield.Briefly, after 500 ms of fixation, a 5-deg natural scene and a red square (3 deg in diameter) were presented simultaneously for the same random duration (1000–1800 ms) at two symmetric locations on the screen. The animal was required to signal the color change for the attended square (from red to green) within the next 3000 ms. Each session consisted of 400 trials. (B) We examined the block-by-block (each block consisted of 100 trials) changes in spike-LFP coherence (SFC) when the image was presented in the neurons' receptive fields (during the first 1000-ms of stimulus presentation). The results (shown as SFC changes with respect to SFC in block 1) confirm the results of our first control experiment (Figure 6A), that is, we were unable to detect significant block-by-block changes in SFC in any frequency band during inattentive (passive) fixation (theta: p = 0.99, alpha: p = 0.21, beta: p = 0.25, gamma: p = 0.49, Kruskal–Wallis test).DOI:http://dx.doi.org/10.7554/eLife.08417.010

Mentions: One important control is to ensure that the changes in theta SFC observed during rapid learning across blocks of trials are not due to the stimulus presentation itself. We thus collected data from one animal in which five control sessions were recorded before the monkey was able to accurately perform the behavioral task with the set of 10 prototype stimuli. However, despite the fact that animals performed a discrimination task identical to that described in Figure 1A and novel stimuli were presented in the same conditions, learning did not take place. Indeed, as shown in Figure 6A (top), for the ‘no learning’ control sessions, behavioral discrimination threshold was high at the beginning of the session (in block 1) and did not undergo statistically significant changes in subsequent blocks (p > 0.1, ANOVA test). Importantly, examining the changes in spike-LFP coherence for the population of 96 pairs, we found that SFC did not change across blocks of trials in any frequency band (p > 0.1, Kruskal–Wallis test, comparing SFC in block 1 vs blocks 2–4). Similar results (no statistically significant block-by-block changes in SFC in any frequency band, Figure 6—figure supplement 1) were found when natural images were flashed in the neurons' receptive fields during passive (inattentive) fixation experiments (n = 12 sessions, 741 pairs). Altogether, these results indicate that the coordination of spike timing with the local theta LFP activity only occurs when animals improve their performance during learning, and that the increase in theta SFC does not continue with subsequent exposure to familiar stimuli after learning has stabilized, or in conditions in which learning does not take place.


Rapid learning in visual cortical networks.

Wang Y, Dragoi V - Elife (2015)

Control experiment—(A) Monkey 2 performed control experiments (n = 12 sessions, 741 cell pairs) in which novel natural scenes were flashed in the neurons' receptive fields, while the animal was engaged in a red/green color detection task in the contralateral hemifield.Briefly, after 500 ms of fixation, a 5-deg natural scene and a red square (3 deg in diameter) were presented simultaneously for the same random duration (1000–1800 ms) at two symmetric locations on the screen. The animal was required to signal the color change for the attended square (from red to green) within the next 3000 ms. Each session consisted of 400 trials. (B) We examined the block-by-block (each block consisted of 100 trials) changes in spike-LFP coherence (SFC) when the image was presented in the neurons' receptive fields (during the first 1000-ms of stimulus presentation). The results (shown as SFC changes with respect to SFC in block 1) confirm the results of our first control experiment (Figure 6A), that is, we were unable to detect significant block-by-block changes in SFC in any frequency band during inattentive (passive) fixation (theta: p = 0.99, alpha: p = 0.21, beta: p = 0.25, gamma: p = 0.49, Kruskal–Wallis test).DOI:http://dx.doi.org/10.7554/eLife.08417.010
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4588715&req=5

fig6s1: Control experiment—(A) Monkey 2 performed control experiments (n = 12 sessions, 741 cell pairs) in which novel natural scenes were flashed in the neurons' receptive fields, while the animal was engaged in a red/green color detection task in the contralateral hemifield.Briefly, after 500 ms of fixation, a 5-deg natural scene and a red square (3 deg in diameter) were presented simultaneously for the same random duration (1000–1800 ms) at two symmetric locations on the screen. The animal was required to signal the color change for the attended square (from red to green) within the next 3000 ms. Each session consisted of 400 trials. (B) We examined the block-by-block (each block consisted of 100 trials) changes in spike-LFP coherence (SFC) when the image was presented in the neurons' receptive fields (during the first 1000-ms of stimulus presentation). The results (shown as SFC changes with respect to SFC in block 1) confirm the results of our first control experiment (Figure 6A), that is, we were unable to detect significant block-by-block changes in SFC in any frequency band during inattentive (passive) fixation (theta: p = 0.99, alpha: p = 0.21, beta: p = 0.25, gamma: p = 0.49, Kruskal–Wallis test).DOI:http://dx.doi.org/10.7554/eLife.08417.010
Mentions: One important control is to ensure that the changes in theta SFC observed during rapid learning across blocks of trials are not due to the stimulus presentation itself. We thus collected data from one animal in which five control sessions were recorded before the monkey was able to accurately perform the behavioral task with the set of 10 prototype stimuli. However, despite the fact that animals performed a discrimination task identical to that described in Figure 1A and novel stimuli were presented in the same conditions, learning did not take place. Indeed, as shown in Figure 6A (top), for the ‘no learning’ control sessions, behavioral discrimination threshold was high at the beginning of the session (in block 1) and did not undergo statistically significant changes in subsequent blocks (p > 0.1, ANOVA test). Importantly, examining the changes in spike-LFP coherence for the population of 96 pairs, we found that SFC did not change across blocks of trials in any frequency band (p > 0.1, Kruskal–Wallis test, comparing SFC in block 1 vs blocks 2–4). Similar results (no statistically significant block-by-block changes in SFC in any frequency band, Figure 6—figure supplement 1) were found when natural images were flashed in the neurons' receptive fields during passive (inattentive) fixation experiments (n = 12 sessions, 741 pairs). Altogether, these results indicate that the coordination of spike timing with the local theta LFP activity only occurs when animals improve their performance during learning, and that the increase in theta SFC does not continue with subsequent exposure to familiar stimuli after learning has stabilized, or in conditions in which learning does not take place.

Bottom Line: We show that the increase in behavioral performance during learning is predicted by a tight coordination of spike timing with local population activity.More spike-LFP theta synchronization is correlated with higher learning performance, while high-frequency synchronization is unrelated with changes in performance, but these changes were absent once learning had stabilized and stimuli became familiar, or in the absence of learning.These findings reveal a novel mechanism of plasticity in visual cortex by which elevated low-frequency synchronization between individual neurons and local population activity accompanies the improvement in performance during learning.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston, Houston, United States.

ABSTRACT
Although changes in brain activity during learning have been extensively examined at the single neuron level, the coding strategies employed by cell populations remain mysterious. We examined cell populations in macaque area V4 during a rapid form of perceptual learning that emerges within tens of minutes. Multiple single units and LFP responses were recorded as monkeys improved their performance in an image discrimination task. We show that the increase in behavioral performance during learning is predicted by a tight coordination of spike timing with local population activity. More spike-LFP theta synchronization is correlated with higher learning performance, while high-frequency synchronization is unrelated with changes in performance, but these changes were absent once learning had stabilized and stimuli became familiar, or in the absence of learning. These findings reveal a novel mechanism of plasticity in visual cortex by which elevated low-frequency synchronization between individual neurons and local population activity accompanies the improvement in performance during learning.

No MeSH data available.


Related in: MedlinePlus