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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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Sequential delayed match-to-sample task.(A) Event sequence. First, a gray fixation spot appears in the center of the screen. Once the monkey fixates on the spot, a sample image replaces the fixation spot for 0.5–1.0 s, after which the spot is restored. After a variable delay-period, the image/spot sequence is repeated 0, 1, 2, or 3 times with nonmatching patterns. Finally, the original (matching) pattern reappears; the monkey has to release the bar within 2 s to get a drop of water as a reward. (ITI, inter-trial interval). (B) Stimuli.
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pcbi-1000073-g001: Sequential delayed match-to-sample task.(A) Event sequence. First, a gray fixation spot appears in the center of the screen. Once the monkey fixates on the spot, a sample image replaces the fixation spot for 0.5–1.0 s, after which the spot is restored. After a variable delay-period, the image/spot sequence is repeated 0, 1, 2, or 3 times with nonmatching patterns. Finally, the original (matching) pattern reappears; the monkey has to release the bar within 2 s to get a drop of water as a reward. (ITI, inter-trial interval). (B) Stimuli.

Mentions: We collected responses from two different parts of ITC: 35 TE neurons and 11 perirhinal neurons from two monkeys performing a visual DMS task (Figure 1A) using eight familiar stimuli (Figure 1B). About 45% of trials had no nonmatch stimuli (sample-match) and about 45% of trials had one nonmatch stimulus (sample-nonmatch-match); the other 10% of trials had two nonmatch stimuli (sample-nonmatch-nonmatch-match) to keep the monkeys attentive to the task. Each picture from the stimulus set was presented as the sample 7–82 times for TE neurons, and 3–82 times for perirhinal neurons. The sample stimulus elicited responses between 0 and 115 spikes/s (median = 10 spikes/s) for TE neurons, and between 0 and 78 spikes/s (median = 10 spikes/s) for perirhinal neurons. In TE, responses were excitatory in 20 neurons, inhibitory in 2 neurons, and either excitatory or inhibitory depending on stimulus pattern in 13 neurons (p<0.05, paired Wilcoxon test). In perirhinal cortex, responses were excitatory in 7 neurons, and were either excitatory or inhibitory depending on stimulus pattern in 4 neurons.


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)

Sequential delayed match-to-sample task.(A) Event sequence. First, a gray fixation spot appears in the center of the screen. Once the monkey fixates on the spot, a sample image replaces the fixation spot for 0.5–1.0 s, after which the spot is restored. After a variable delay-period, the image/spot sequence is repeated 0, 1, 2, or 3 times with nonmatching patterns. Finally, the original (matching) pattern reappears; the monkey has to release the bar within 2 s to get a drop of water as a reward. (ITI, inter-trial interval). (B) Stimuli.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2366068&req=5

pcbi-1000073-g001: Sequential delayed match-to-sample task.(A) Event sequence. First, a gray fixation spot appears in the center of the screen. Once the monkey fixates on the spot, a sample image replaces the fixation spot for 0.5–1.0 s, after which the spot is restored. After a variable delay-period, the image/spot sequence is repeated 0, 1, 2, or 3 times with nonmatching patterns. Finally, the original (matching) pattern reappears; the monkey has to release the bar within 2 s to get a drop of water as a reward. (ITI, inter-trial interval). (B) Stimuli.
Mentions: We collected responses from two different parts of ITC: 35 TE neurons and 11 perirhinal neurons from two monkeys performing a visual DMS task (Figure 1A) using eight familiar stimuli (Figure 1B). About 45% of trials had no nonmatch stimuli (sample-match) and about 45% of trials had one nonmatch stimulus (sample-nonmatch-match); the other 10% of trials had two nonmatch stimuli (sample-nonmatch-nonmatch-match) to keep the monkeys attentive to the task. Each picture from the stimulus set was presented as the sample 7–82 times for TE neurons, and 3–82 times for perirhinal neurons. The sample stimulus elicited responses between 0 and 115 spikes/s (median = 10 spikes/s) for TE neurons, and between 0 and 78 spikes/s (median = 10 spikes/s) for perirhinal neurons. In TE, responses were excitatory in 20 neurons, inhibitory in 2 neurons, and either excitatory or inhibitory depending on stimulus pattern in 13 neurons (p<0.05, paired Wilcoxon test). In perirhinal cortex, responses were excitatory in 7 neurons, and were either excitatory or inhibitory depending on stimulus pattern in 4 neurons.

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