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Short-term memory trace in rapidly adapting synapses of inferior temporal cortex.

Sugase-Miyamoto Y, Liu Z, Wiener MC, Optican LM, Richmond BJ - PLoS Comput. Biol. (2008)

Bottom Line: We found that a large proportion (80%) of stimulus-selective neurons in area TE of macaque ITCs exhibit a memory effect during the stimulus interval.Neurons in perirhinal cortex did not show this correlation.Simulations of a matched filter model match the experimental results, suggesting that area TE neurons store a synaptic memory trace during short-term visual memory.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland, United States of America.

ABSTRACT
Visual short-term memory tasks depend upon both the inferior temporal cortex (ITC) and the prefrontal cortex (PFC). Activity in some neurons persists after the first (sample) stimulus is shown. This delay-period activity has been proposed as an important mechanism for working memory. In ITC neurons, intervening (nonmatching) stimuli wipe out the delay-period activity; hence, the role of ITC in memory must depend upon a different mechanism. Here, we look for a possible mechanism by contrasting memory effects in two architectonically different parts of ITC: area TE and the perirhinal cortex. We found that a large proportion (80%) of stimulus-selective neurons in area TE of macaque ITCs exhibit a memory effect during the stimulus interval. During a sequential delayed matching-to-sample task (DMS), the noise in the neuronal response to the test image was correlated with the noise in the neuronal response to the sample image. Neurons in perirhinal cortex did not show this correlation. These results led us to hypothesize that area TE contributes to short-term memory by acting as a matched filter. When the sample image appears, each TE neuron captures a static copy of its inputs by rapidly adjusting its synaptic weights to match the strength of their individual inputs. Input signals from subsequent images are multiplied by those synaptic weights, thereby computing a measure of the correlation between the past and present inputs. The total activity in area TE is sufficient to quantify the similarity between the two images. This matched filter theory provides an explanation of what is remembered, where the trace is stored, and how comparison is done across time, all without requiring delay period activity. Simulations of a matched filter model match the experimental results, suggesting that area TE neurons store a synaptic memory trace during short-term visual memory.

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Performance on the DMS task of the deterministic matched filter model.(A) Performance of the deterministic matched filter model using the data from the recorded sample of 35 TE neurons. The left column shows the eight stimuli presented to the model as the sample, and the top row shows the eight stimuli presented as the test image. At the intersection of each row and column is the average response of all the estimates across 35 TE neurons using the matched filter model. The upper-left to lower-right diagonal shows the matched filter outputs for the eight sample-match pairs. The off diagonals show the matched filter outputs for the 56 sample-nonmatch pairs. The model gave the best discrimination performance with the threshold set to 6.15 spikes per 400 ms epoch, i.e., the model made the fewest mistakes. The blue values show correct matches (hits), and the green responses show the correct nonmatches (correct rejections). The orange values show misses, and the red values show false alarms. This model got 32/64 = 50% of the trials correct. (B) Performance of the matched filter model for perirhinal neurons with inputs from encoder stage estimate. At the intersection of each row and column is the average response of all the estimates across 11 perirhinal neurons using the matched filter model. With the threshold set to 4.55 spikes per 400 ms epoch, the model achieved its best performance, getting 35/64 = 55% of the trials correct.
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pcbi-1000073-g007: Performance on the DMS task of the deterministic matched filter model.(A) Performance of the deterministic matched filter model using the data from the recorded sample of 35 TE neurons. The left column shows the eight stimuli presented to the model as the sample, and the top row shows the eight stimuli presented as the test image. At the intersection of each row and column is the average response of all the estimates across 35 TE neurons using the matched filter model. The upper-left to lower-right diagonal shows the matched filter outputs for the eight sample-match pairs. The off diagonals show the matched filter outputs for the 56 sample-nonmatch pairs. The model gave the best discrimination performance with the threshold set to 6.15 spikes per 400 ms epoch, i.e., the model made the fewest mistakes. The blue values show correct matches (hits), and the green responses show the correct nonmatches (correct rejections). The orange values show misses, and the red values show false alarms. This model got 32/64 = 50% of the trials correct. (B) Performance of the matched filter model for perirhinal neurons with inputs from encoder stage estimate. At the intersection of each row and column is the average response of all the estimates across 11 perirhinal neurons using the matched filter model. With the threshold set to 4.55 spikes per 400 ms epoch, the model achieved its best performance, getting 35/64 = 55% of the trials correct.

Mentions: Figure 7A shows the results of computing the match-nonmatch performance for the set of 64 population responses for the 35 TE neurons. Each row (sample) and column (test) begins with the corresponding stimulus. The average population response is printed for each nonmatch and match decision. The diagonal values show the match responses (in spikes per 400 ms epoch). A number colored in blue is a correct match decision (or hit, based on a threshold of 6.15), and an orange number is a miss. The off-diagonal elements show the nonmatch responses. A green number is a correct rejection, and a red number is a false alarm. Overall, the matched filter based on these 35 neurons scored 50% correct (ROC d' = 1.02; random would have been 1/64 or 1.56% correct) on the DMS task. The same comparison is made in Figure 7B for the perirhinal neurons, which scored 55% correct (d' = 0.72). The similarity in scores is not surprising, as TE neurons project to perirhinal cortex. However, the d' value (which is the separation of the means of the probability density functions of occurrence, with and without signal, divided by the standard deviation of the distributions) is much smaller in perirhinal neurons. This suggests that signals that were separate in TE have become confounded in perirhinal cortex.


Short-term memory trace in rapidly adapting synapses of inferior temporal cortex.

Sugase-Miyamoto Y, Liu Z, Wiener MC, Optican LM, Richmond BJ - PLoS Comput. Biol. (2008)

Performance on the DMS task of the deterministic matched filter model.(A) Performance of the deterministic matched filter model using the data from the recorded sample of 35 TE neurons. The left column shows the eight stimuli presented to the model as the sample, and the top row shows the eight stimuli presented as the test image. At the intersection of each row and column is the average response of all the estimates across 35 TE neurons using the matched filter model. The upper-left to lower-right diagonal shows the matched filter outputs for the eight sample-match pairs. The off diagonals show the matched filter outputs for the 56 sample-nonmatch pairs. The model gave the best discrimination performance with the threshold set to 6.15 spikes per 400 ms epoch, i.e., the model made the fewest mistakes. The blue values show correct matches (hits), and the green responses show the correct nonmatches (correct rejections). The orange values show misses, and the red values show false alarms. This model got 32/64 = 50% of the trials correct. (B) Performance of the matched filter model for perirhinal neurons with inputs from encoder stage estimate. At the intersection of each row and column is the average response of all the estimates across 11 perirhinal neurons using the matched filter model. With the threshold set to 4.55 spikes per 400 ms epoch, the model achieved its best performance, getting 35/64 = 55% of the trials correct.
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Related In: Results  -  Collection

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pcbi-1000073-g007: Performance on the DMS task of the deterministic matched filter model.(A) Performance of the deterministic matched filter model using the data from the recorded sample of 35 TE neurons. The left column shows the eight stimuli presented to the model as the sample, and the top row shows the eight stimuli presented as the test image. At the intersection of each row and column is the average response of all the estimates across 35 TE neurons using the matched filter model. The upper-left to lower-right diagonal shows the matched filter outputs for the eight sample-match pairs. The off diagonals show the matched filter outputs for the 56 sample-nonmatch pairs. The model gave the best discrimination performance with the threshold set to 6.15 spikes per 400 ms epoch, i.e., the model made the fewest mistakes. The blue values show correct matches (hits), and the green responses show the correct nonmatches (correct rejections). The orange values show misses, and the red values show false alarms. This model got 32/64 = 50% of the trials correct. (B) Performance of the matched filter model for perirhinal neurons with inputs from encoder stage estimate. At the intersection of each row and column is the average response of all the estimates across 11 perirhinal neurons using the matched filter model. With the threshold set to 4.55 spikes per 400 ms epoch, the model achieved its best performance, getting 35/64 = 55% of the trials correct.
Mentions: Figure 7A shows the results of computing the match-nonmatch performance for the set of 64 population responses for the 35 TE neurons. Each row (sample) and column (test) begins with the corresponding stimulus. The average population response is printed for each nonmatch and match decision. The diagonal values show the match responses (in spikes per 400 ms epoch). A number colored in blue is a correct match decision (or hit, based on a threshold of 6.15), and an orange number is a miss. The off-diagonal elements show the nonmatch responses. A green number is a correct rejection, and a red number is a false alarm. Overall, the matched filter based on these 35 neurons scored 50% correct (ROC d' = 1.02; random would have been 1/64 or 1.56% correct) on the DMS task. The same comparison is made in Figure 7B for the perirhinal neurons, which scored 55% correct (d' = 0.72). The similarity in scores is not surprising, as TE neurons project to perirhinal cortex. However, the d' value (which is the separation of the means of the probability density functions of occurrence, with and without signal, divided by the standard deviation of the distributions) is much smaller in perirhinal neurons. This suggests that signals that were separate in TE have become confounded in perirhinal cortex.

Bottom Line: We found that a large proportion (80%) of stimulus-selective neurons in area TE of macaque ITCs exhibit a memory effect during the stimulus interval.Neurons in perirhinal cortex did not show this correlation.Simulations of a matched filter model match the experimental results, suggesting that area TE neurons store a synaptic memory trace during short-term visual memory.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland, United States of America.

ABSTRACT
Visual short-term memory tasks depend upon both the inferior temporal cortex (ITC) and the prefrontal cortex (PFC). Activity in some neurons persists after the first (sample) stimulus is shown. This delay-period activity has been proposed as an important mechanism for working memory. In ITC neurons, intervening (nonmatching) stimuli wipe out the delay-period activity; hence, the role of ITC in memory must depend upon a different mechanism. Here, we look for a possible mechanism by contrasting memory effects in two architectonically different parts of ITC: area TE and the perirhinal cortex. We found that a large proportion (80%) of stimulus-selective neurons in area TE of macaque ITCs exhibit a memory effect during the stimulus interval. During a sequential delayed matching-to-sample task (DMS), the noise in the neuronal response to the test image was correlated with the noise in the neuronal response to the sample image. Neurons in perirhinal cortex did not show this correlation. These results led us to hypothesize that area TE contributes to short-term memory by acting as a matched filter. When the sample image appears, each TE neuron captures a static copy of its inputs by rapidly adjusting its synaptic weights to match the strength of their individual inputs. Input signals from subsequent images are multiplied by those synaptic weights, thereby computing a measure of the correlation between the past and present inputs. The total activity in area TE is sufficient to quantify the similarity between the two images. This matched filter theory provides an explanation of what is remembered, where the trace is stored, and how comparison is done across time, all without requiring delay period activity. Simulations of a matched filter model match the experimental results, suggesting that area TE neurons store a synaptic memory trace during short-term visual memory.

Show MeSH
Related in: MedlinePlus