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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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Response variance explained by stimulus identity, demonstrating that these cells were stimulus selective.(A) Percentage of variance explained by stimulus identity in the sample, nonmatch, and match task phases for the population of 35 TE neurons, and for the population of 11 perirhinal cortex neurons. In box plots, the middle line indicates the median. The notches indicate the 95% confidence interval for the median. The whiskers extend to the most extreme data point which is no more than 1.5 times the inter-quartile range from the box. Population distributions across both TE and perirhinal cortex explained the same amount of variance in the sample, nonmatch and match phases. However, in some cells, the behavioral phase significantly influenced the response magnitude. (B) percentage of variance explained by sample stimulus identity in a 200-ms delay period before nonmatch stimulus presentation (Delay(NM)), and before match stimulus presentation (Delay(M)).
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pcbi-1000073-g002: Response variance explained by stimulus identity, demonstrating that these cells were stimulus selective.(A) Percentage of variance explained by stimulus identity in the sample, nonmatch, and match task phases for the population of 35 TE neurons, and for the population of 11 perirhinal cortex neurons. In box plots, the middle line indicates the median. The notches indicate the 95% confidence interval for the median. The whiskers extend to the most extreme data point which is no more than 1.5 times the inter-quartile range from the box. Population distributions across both TE and perirhinal cortex explained the same amount of variance in the sample, nonmatch and match phases. However, in some cells, the behavioral phase significantly influenced the response magnitude. (B) percentage of variance explained by sample stimulus identity in a 200-ms delay period before nonmatch stimulus presentation (Delay(NM)), and before match stimulus presentation (Delay(M)).

Mentions: The stimulus-elicited responses of both TE and perirhinal neurons were stimulus selective, as expected [12],[13],[39]. In area TE, the effect of the stimulus identity was significant in the sample, nonmatch, and match phases for 29, 34, and 32 of the 35 neurons, respectively (Figure 2A; response variance explained; 1-way ANOVA, p<0.05). In perirhinal cortex, the effect of the stimulus identity was significant in the sample, nonmatch, and match phases for 9, 9, and 8 of the 11 neurons, respectively. Stimulus selectivity explained 26% (mean) of the response variance in TE, and 13% in perirhinal neurons (Figure 2A).


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)

Response variance explained by stimulus identity, demonstrating that these cells were stimulus selective.(A) Percentage of variance explained by stimulus identity in the sample, nonmatch, and match task phases for the population of 35 TE neurons, and for the population of 11 perirhinal cortex neurons. In box plots, the middle line indicates the median. The notches indicate the 95% confidence interval for the median. The whiskers extend to the most extreme data point which is no more than 1.5 times the inter-quartile range from the box. Population distributions across both TE and perirhinal cortex explained the same amount of variance in the sample, nonmatch and match phases. However, in some cells, the behavioral phase significantly influenced the response magnitude. (B) percentage of variance explained by sample stimulus identity in a 200-ms delay period before nonmatch stimulus presentation (Delay(NM)), and before match stimulus presentation (Delay(M)).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2366068&req=5

pcbi-1000073-g002: Response variance explained by stimulus identity, demonstrating that these cells were stimulus selective.(A) Percentage of variance explained by stimulus identity in the sample, nonmatch, and match task phases for the population of 35 TE neurons, and for the population of 11 perirhinal cortex neurons. In box plots, the middle line indicates the median. The notches indicate the 95% confidence interval for the median. The whiskers extend to the most extreme data point which is no more than 1.5 times the inter-quartile range from the box. Population distributions across both TE and perirhinal cortex explained the same amount of variance in the sample, nonmatch and match phases. However, in some cells, the behavioral phase significantly influenced the response magnitude. (B) percentage of variance explained by sample stimulus identity in a 200-ms delay period before nonmatch stimulus presentation (Delay(NM)), and before match stimulus presentation (Delay(M)).
Mentions: The stimulus-elicited responses of both TE and perirhinal neurons were stimulus selective, as expected [12],[13],[39]. In area TE, the effect of the stimulus identity was significant in the sample, nonmatch, and match phases for 29, 34, and 32 of the 35 neurons, respectively (Figure 2A; response variance explained; 1-way ANOVA, p<0.05). In perirhinal cortex, the effect of the stimulus identity was significant in the sample, nonmatch, and match phases for 9, 9, and 8 of the 11 neurons, respectively. Stimulus selectivity explained 26% (mean) of the response variance in TE, and 13% in perirhinal neurons (Figure 2A).

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