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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 of the matched filter across full set of stimulus pairs by the stochastic model simulation.The left column shows the 8 stimuli presented to the model as the sample, and the top row shows the 8 stimuli presented as a match or nonmatch. The intersection of each row and column is a 16×16 pixel image made up of the responses of the 256 model TE neurons. The diagonal (with slope -1) 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 total power (normalized to 1.0 for the peak of the 64 pair set, in this example, S7-S7 sample-match) is shown above each output. With the threshold set to 0.225, the model made the fewest mistakes (false alarms, red values). The green values show correct matches, and the blue responses show the correct nonmatches. With the noise in the model adjusted to match that in the monkeys, the model got 62/64 = 97% of the trials correct. The average performance across the two monkeys was 98%.
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pcbi-1000073-g009: Performance of the matched filter across full set of stimulus pairs by the stochastic model simulation.The left column shows the 8 stimuli presented to the model as the sample, and the top row shows the 8 stimuli presented as a match or nonmatch. The intersection of each row and column is a 16×16 pixel image made up of the responses of the 256 model TE neurons. The diagonal (with slope -1) 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 total power (normalized to 1.0 for the peak of the 64 pair set, in this example, S7-S7 sample-match) is shown above each output. With the threshold set to 0.225, the model made the fewest mistakes (false alarms, red values). The green values show correct matches, and the blue responses show the correct nonmatches. With the noise in the model adjusted to match that in the monkeys, the model got 62/64 = 97% of the trials correct. The average performance across the two monkeys was 98%.

Mentions: The output results for all 64 combinations of stimulus and test patterns are shown in Figure 9. As in Figure 7, the matches are on the diagonal, and the nonmatches are on the off-diagonals. The normalized output power is printed above each response image for a population of 256 encoder neurons (shown as a 16×16 icon). Green numbers are correct hits, blue are correct rejections, orange are misses (none in this example), and red are false alarms. With the threshold set to 0.225, the model makes only two mistakes (both false alarms). This gives the model a success rate of 97% (d' = 3.34; the correction for p(hit) = 1 was made using p(hit) = 1−0.5/(Nhit+Nmiss), [41]). The average success rate of our two monkeys was 98%. (These two rates are so close because the noise in the model was tuned to match these monkeys, so it is a fit, not a prediction; see Methods).


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 of the matched filter across full set of stimulus pairs by the stochastic model simulation.The left column shows the 8 stimuli presented to the model as the sample, and the top row shows the 8 stimuli presented as a match or nonmatch. The intersection of each row and column is a 16×16 pixel image made up of the responses of the 256 model TE neurons. The diagonal (with slope -1) 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 total power (normalized to 1.0 for the peak of the 64 pair set, in this example, S7-S7 sample-match) is shown above each output. With the threshold set to 0.225, the model made the fewest mistakes (false alarms, red values). The green values show correct matches, and the blue responses show the correct nonmatches. With the noise in the model adjusted to match that in the monkeys, the model got 62/64 = 97% of the trials correct. The average performance across the two monkeys was 98%.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2366068&req=5

pcbi-1000073-g009: Performance of the matched filter across full set of stimulus pairs by the stochastic model simulation.The left column shows the 8 stimuli presented to the model as the sample, and the top row shows the 8 stimuli presented as a match or nonmatch. The intersection of each row and column is a 16×16 pixel image made up of the responses of the 256 model TE neurons. The diagonal (with slope -1) 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 total power (normalized to 1.0 for the peak of the 64 pair set, in this example, S7-S7 sample-match) is shown above each output. With the threshold set to 0.225, the model made the fewest mistakes (false alarms, red values). The green values show correct matches, and the blue responses show the correct nonmatches. With the noise in the model adjusted to match that in the monkeys, the model got 62/64 = 97% of the trials correct. The average performance across the two monkeys was 98%.
Mentions: The output results for all 64 combinations of stimulus and test patterns are shown in Figure 9. As in Figure 7, the matches are on the diagonal, and the nonmatches are on the off-diagonals. The normalized output power is printed above each response image for a population of 256 encoder neurons (shown as a 16×16 icon). Green numbers are correct hits, blue are correct rejections, orange are misses (none in this example), and red are false alarms. With the threshold set to 0.225, the model makes only two mistakes (both false alarms). This gives the model a success rate of 97% (d' = 3.34; the correction for p(hit) = 1 was made using p(hit) = 1−0.5/(Nhit+Nmiss), [41]). The average success rate of our two monkeys was 98%. (These two rates are so close because the noise in the model was tuned to match these monkeys, so it is a fit, not a prediction; see Methods).

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