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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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Correlations of response deviations.(A, B) Correlations between sample versus match (filled circles, solid line) and sample versus nonmatch response deviations (open circles, broken line) for one TE (A) and one perirhinal neuron (B). The correlation for sample vs. match is significantly different than for sample versus nonmatch deviations in (A) (Z statistic = 2.11, df = 366, p = 0.018). (C, D) Mean±SE of variance of response deviations explained by TE (C) and perirhinal (D) populations. Differences between sample vs. match and other comparisons (either gray versus either white bar) were significant only in TE (paired t-test, p<0.05).
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pcbi-1000073-g003: Correlations of response deviations.(A, B) Correlations between sample versus match (filled circles, solid line) and sample versus nonmatch response deviations (open circles, broken line) for one TE (A) and one perirhinal neuron (B). The correlation for sample vs. match is significantly different than for sample versus nonmatch deviations in (A) (Z statistic = 2.11, df = 366, p = 0.018). (C, D) Mean±SE of variance of response deviations explained by TE (C) and perirhinal (D) populations. Differences between sample vs. match and other comparisons (either gray versus either white bar) were significant only in TE (paired t-test, p<0.05).

Mentions: To quantify the response variation (noise), the phase- and stimulus-dependent mean spike count for each neuron was subtracted from the spike count on each trial in the corresponding task phase. These residuals (noise) were not dependent on the stimulus (1-way ANOVA). However, the deviations during different task phases were correlated with each other, that is, when the response to the sample was above the mean, the response to the match was also likely to be above the mean. On a cell-by-cell basis, the correlations between the sample vs. match deviations were greater than the correlations between the sample vs. nonmatch deviations for most (28/35 = 80%) of the TE neurons (cf. example neuron in Figure 3A). In the sample-nonmatch-match trials, the correlation between deviations for sample and nonmatch images (variance accounted for by linear regression, R2 = 7.5±1.8%, N = 35) was weaker than the correlation between deviations in sample-match trials with no intervening nonmatch image (R2 = 13.4±2.5%, N = 35; Figure 3C; paired t-test, p<0.05). Thus, for periods separated by the same amount of time, sample-match correlations are stronger than sample-nonmatch correlations.


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)

Correlations of response deviations.(A, B) Correlations between sample versus match (filled circles, solid line) and sample versus nonmatch response deviations (open circles, broken line) for one TE (A) and one perirhinal neuron (B). The correlation for sample vs. match is significantly different than for sample versus nonmatch deviations in (A) (Z statistic = 2.11, df = 366, p = 0.018). (C, D) Mean±SE of variance of response deviations explained by TE (C) and perirhinal (D) populations. Differences between sample vs. match and other comparisons (either gray versus either white bar) were significant only in TE (paired t-test, p<0.05).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2366068&req=5

pcbi-1000073-g003: Correlations of response deviations.(A, B) Correlations between sample versus match (filled circles, solid line) and sample versus nonmatch response deviations (open circles, broken line) for one TE (A) and one perirhinal neuron (B). The correlation for sample vs. match is significantly different than for sample versus nonmatch deviations in (A) (Z statistic = 2.11, df = 366, p = 0.018). (C, D) Mean±SE of variance of response deviations explained by TE (C) and perirhinal (D) populations. Differences between sample vs. match and other comparisons (either gray versus either white bar) were significant only in TE (paired t-test, p<0.05).
Mentions: To quantify the response variation (noise), the phase- and stimulus-dependent mean spike count for each neuron was subtracted from the spike count on each trial in the corresponding task phase. These residuals (noise) were not dependent on the stimulus (1-way ANOVA). However, the deviations during different task phases were correlated with each other, that is, when the response to the sample was above the mean, the response to the match was also likely to be above the mean. On a cell-by-cell basis, the correlations between the sample vs. match deviations were greater than the correlations between the sample vs. nonmatch deviations for most (28/35 = 80%) of the TE neurons (cf. example neuron in Figure 3A). In the sample-nonmatch-match trials, the correlation between deviations for sample and nonmatch images (variance accounted for by linear regression, R2 = 7.5±1.8%, N = 35) was weaker than the correlation between deviations in sample-match trials with no intervening nonmatch image (R2 = 13.4±2.5%, N = 35; Figure 3C; paired t-test, p<0.05). Thus, for periods separated by the same amount of time, sample-match correlations are stronger than sample-nonmatch correlations.

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