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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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Schematic localization of recording sites.(A) Ventral view of the brain with perirhinal cortex (medial, dots) and area TE (hatched) highlighted. Actual recording was done in parts of area TE and perirhinal cortex that are indicated in gray. (B) Coronal cross-section of a standard rhesus monkey atlas (Laboratory of Neuropsychology, NIMH; http://ln.nimh.nih.gov/) at 17 mm rostral to the interaural line (AP +17) showing a recording track into perirhinal cortex and a track into area TE. The noise correlation was found to occur for most area TE neurons that were recorded lateral to the anterior middle temporal sulcus. The noise correlation was not found in the responses of neurons recorded in perirhinal cortex in this or pervious studies recorded medial to anterior middle temporal sulcus [19],[45]. MRs with electrodes can be seen in Liu and Richmond [13]. amts, anterior middle temporal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus; TE, area TE; Prh, perirhinal cortex.
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pcbi-1000073-g012: Schematic localization of recording sites.(A) Ventral view of the brain with perirhinal cortex (medial, dots) and area TE (hatched) highlighted. Actual recording was done in parts of area TE and perirhinal cortex that are indicated in gray. (B) Coronal cross-section of a standard rhesus monkey atlas (Laboratory of Neuropsychology, NIMH; http://ln.nimh.nih.gov/) at 17 mm rostral to the interaural line (AP +17) showing a recording track into perirhinal cortex and a track into area TE. The noise correlation was found to occur for most area TE neurons that were recorded lateral to the anterior middle temporal sulcus. The noise correlation was not found in the responses of neurons recorded in perirhinal cortex in this or pervious studies recorded medial to anterior middle temporal sulcus [19],[45]. MRs with electrodes can be seen in Liu and Richmond [13]. amts, anterior middle temporal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus; TE, area TE; Prh, perirhinal cortex.

Mentions: As information has been collected about localization of memory functions in the brain over the past decade, it has become clear that different architectonic regions of inferior temporal cortex have different functional roles in memory, specifically the lateral inferior temporal area TE has different roles in memory than the more medial inferior temporal perirhinal cortex [10],[11],[42],[43]. Among other differences bilateral ablation of the more lateral area TE interferes with memory at all delays whereas damage to the more medial perirhinal cortex interferes with memory only after longer delays in monkeys [11]. This suggests that area TE is involved in the initial encoding of information for memory formation in general. Relevant to the present study, neurons in both areas show stimulus selectivity, and activity related to stimulus-stimulus associations [43]. However, the stimulus-stimulus association related activity in TE is dependent on perirhinal cortex [44]. Latencies of the visual stimulus elicited responses are considerably shorter in area TE than in perirhinal cortex, and stimulus-elicited reward schedule related selectivity arising from associative learning is seen in perirhinal neurons, but not in area TE neurons [13]. Here, we found that the stimulus-elicited responses recorded between anterior middle temporal sulcus and superior temporal sulcus, area TE (Figure 12), have a short-term memory related signal, and that neurons recorded medial to anterior middle temporal sulcus and lateral to rhinal sulcus, perihinal cortex and perhaps medial area TE, do not have this signal. Our findings in perirhinal cortex are consistent with previous findings in perirhinal cortex [19],[45].


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)

Schematic localization of recording sites.(A) Ventral view of the brain with perirhinal cortex (medial, dots) and area TE (hatched) highlighted. Actual recording was done in parts of area TE and perirhinal cortex that are indicated in gray. (B) Coronal cross-section of a standard rhesus monkey atlas (Laboratory of Neuropsychology, NIMH; http://ln.nimh.nih.gov/) at 17 mm rostral to the interaural line (AP +17) showing a recording track into perirhinal cortex and a track into area TE. The noise correlation was found to occur for most area TE neurons that were recorded lateral to the anterior middle temporal sulcus. The noise correlation was not found in the responses of neurons recorded in perirhinal cortex in this or pervious studies recorded medial to anterior middle temporal sulcus [19],[45]. MRs with electrodes can be seen in Liu and Richmond [13]. amts, anterior middle temporal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus; TE, area TE; Prh, perirhinal cortex.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2366068&req=5

pcbi-1000073-g012: Schematic localization of recording sites.(A) Ventral view of the brain with perirhinal cortex (medial, dots) and area TE (hatched) highlighted. Actual recording was done in parts of area TE and perirhinal cortex that are indicated in gray. (B) Coronal cross-section of a standard rhesus monkey atlas (Laboratory of Neuropsychology, NIMH; http://ln.nimh.nih.gov/) at 17 mm rostral to the interaural line (AP +17) showing a recording track into perirhinal cortex and a track into area TE. The noise correlation was found to occur for most area TE neurons that were recorded lateral to the anterior middle temporal sulcus. The noise correlation was not found in the responses of neurons recorded in perirhinal cortex in this or pervious studies recorded medial to anterior middle temporal sulcus [19],[45]. MRs with electrodes can be seen in Liu and Richmond [13]. amts, anterior middle temporal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus; TE, area TE; Prh, perirhinal cortex.
Mentions: As information has been collected about localization of memory functions in the brain over the past decade, it has become clear that different architectonic regions of inferior temporal cortex have different functional roles in memory, specifically the lateral inferior temporal area TE has different roles in memory than the more medial inferior temporal perirhinal cortex [10],[11],[42],[43]. Among other differences bilateral ablation of the more lateral area TE interferes with memory at all delays whereas damage to the more medial perirhinal cortex interferes with memory only after longer delays in monkeys [11]. This suggests that area TE is involved in the initial encoding of information for memory formation in general. Relevant to the present study, neurons in both areas show stimulus selectivity, and activity related to stimulus-stimulus associations [43]. However, the stimulus-stimulus association related activity in TE is dependent on perirhinal cortex [44]. Latencies of the visual stimulus elicited responses are considerably shorter in area TE than in perirhinal cortex, and stimulus-elicited reward schedule related selectivity arising from associative learning is seen in perirhinal neurons, but not in area TE neurons [13]. Here, we found that the stimulus-elicited responses recorded between anterior middle temporal sulcus and superior temporal sulcus, area TE (Figure 12), have a short-term memory related signal, and that neurons recorded medial to anterior middle temporal sulcus and lateral to rhinal sulcus, perihinal cortex and perhaps medial area TE, do not have this signal. Our findings in perirhinal cortex are consistent with previous findings in perirhinal cortex [19],[45].

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