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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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Stochastic model's noise correlations.Correlations for noise in sample versus match and sample versus nonmatch deviations are similar to our data. (A, B) TE shows significantly higher noise correlations for sample versus match phases. (C, D) response deviations in the perirhinal cortex are much less, and more uniformly, correlated. Data are from trials with no intervening nonmatch stimuli for sample versus match or from trials with one nonmatch stimulus for sample versus nonmatch. Uniform correlations in perirhinal cortex are due to slowly varying input noise. Increased sample versus match noise correlations depend on a multiplicative interaction between memory trace and current input.
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pcbi-1000073-g010: Stochastic model's noise correlations.Correlations for noise in sample versus match and sample versus nonmatch deviations are similar to our data. (A, B) TE shows significantly higher noise correlations for sample versus match phases. (C, D) response deviations in the perirhinal cortex are much less, and more uniformly, correlated. Data are from trials with no intervening nonmatch stimuli for sample versus match or from trials with one nonmatch stimulus for sample versus nonmatch. Uniform correlations in perirhinal cortex are due to slowly varying input noise. Increased sample versus match noise correlations depend on a multiplicative interaction between memory trace and current input.

Mentions: A quantitative comparison of the performance of the model with that of the monkeys is shown in Figure 10. The average correlations between the sample and match response deviations are shown for actual and simulated TE neuronal responses (Figure 10A and 10B, respectively). The response correlation was larger between the sample and match phase than between the sample and nonmatch phase (for simulated response: paired t-test, p≤0.00001; for actual response: p< = 0.001). As a control, the same model was used to simulate a population of neurons in perirhinal cortex by fixing the synaptic weights (Figure 4, Wkm) to 1.0. Without synaptic plasticity, noise correlations in the perirhinal simulations were the same for all phase pairs (Figure 10D), as was found in the experimental data (Figure 10C). Thus, our simple matched filter model shows that the unexpected correlation between noises at different times for sample vs. match responses is an emergent property of a multiplicative matched filter model that stores its memory trace locally with one-trial learning of synaptic weights.


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)

Stochastic model's noise correlations.Correlations for noise in sample versus match and sample versus nonmatch deviations are similar to our data. (A, B) TE shows significantly higher noise correlations for sample versus match phases. (C, D) response deviations in the perirhinal cortex are much less, and more uniformly, correlated. Data are from trials with no intervening nonmatch stimuli for sample versus match or from trials with one nonmatch stimulus for sample versus nonmatch. Uniform correlations in perirhinal cortex are due to slowly varying input noise. Increased sample versus match noise correlations depend on a multiplicative interaction between memory trace and current input.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2366068&req=5

pcbi-1000073-g010: Stochastic model's noise correlations.Correlations for noise in sample versus match and sample versus nonmatch deviations are similar to our data. (A, B) TE shows significantly higher noise correlations for sample versus match phases. (C, D) response deviations in the perirhinal cortex are much less, and more uniformly, correlated. Data are from trials with no intervening nonmatch stimuli for sample versus match or from trials with one nonmatch stimulus for sample versus nonmatch. Uniform correlations in perirhinal cortex are due to slowly varying input noise. Increased sample versus match noise correlations depend on a multiplicative interaction between memory trace and current input.
Mentions: A quantitative comparison of the performance of the model with that of the monkeys is shown in Figure 10. The average correlations between the sample and match response deviations are shown for actual and simulated TE neuronal responses (Figure 10A and 10B, respectively). The response correlation was larger between the sample and match phase than between the sample and nonmatch phase (for simulated response: paired t-test, p≤0.00001; for actual response: p< = 0.001). As a control, the same model was used to simulate a population of neurons in perirhinal cortex by fixing the synaptic weights (Figure 4, Wkm) to 1.0. Without synaptic plasticity, noise correlations in the perirhinal simulations were the same for all phase pairs (Figure 10D), as was found in the experimental data (Figure 10C). Thus, our simple matched filter model shows that the unexpected correlation between noises at different times for sample vs. match responses is an emergent property of a multiplicative matched filter model that stores its memory trace locally with one-trial learning of synaptic weights.

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