Human medial temporal lobe neurons respond preferentially to personally relevant images

Human medial temporal lobe neurons respond preferentially to personally relevant images Viskontas Quiroga Fried

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Human medial temporal lobe neurons respond preferentially to personally relevant images 2009 Proceedings of the National Academy of Sciences 10.1073/pnas.0902319106 Viskontas2009-human-medial-temporal-lobe-neurons-respond-p Viskontas2009-human-medial-temporal-lobe-neurons-respond-p.txt, the project's staged copy c2566df43b26b220bea383eeb4f0e7d731afae07 not-redistributable neuroscience

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0 spans located by searching the stored text for the quote's exact words, allowing any whitespace between them whether single neurons in the human medial temporal lobe are more likely to respond selectively to images that are personally relevant to the patient Quotation withheld because this record is not cleared for redistribution. does personal relevance make a stimulus more likely to recruit a selective excitatory response from an MTL cell Quotation withheld because this record is not cleared for redistribution. grades selective MTL responsiveness by personal relevance — experimenters and family highest, celebrities intermediate, unknown faces lowest — and finds the gradient differs by MTL region Quotation withheld because this record is not cleared for redistribution. existence Quotation withheld because this record is not cleared for redistribution. personal relevance in human medial temporal lobe single-neuron responses Quotation withheld because this record is not cleared for redistribution. electrophysiology electrophysiology Quotation withheld because this record is not cleared for redistribution. mechanisms Personally relevant images are linked to more, and more varied, past experiences, so a larger number of MTL neurons are recruited to encode them Quotation withheld because this record is not cleared for redistribution. mechanisms Viewing a familiar face activates a richer network of associations than an unfamiliar one, and that richer network is what drives extra MTL cells into responding Quotation withheld because this record is not cleared for redistribution. mechanisms Incidental (unintentional) recollection of the autobiographical network attached to an item is the route by which personal relevance enhances encoding Quotation withheld because this record is not cleared for redistribution. mechanisms In the amygdala the driver is not personal relevance but a combination of novelty and emotional significance, which is why recently met experimenters outrank long-known family members there Quotation withheld because this record is not cleared for redistribution. the experimenters themselves are used as a stimulus category, which manufactures personal relevance the authors control rather than having to find it Quotation withheld because this record is not cleared for redistribution. relevance is turned into an ordered scale — unknown, famous, family, experimenter — so the prediction is a gradient rather than a single contrast Quotation withheld because this record is not cleared for redistribution. selectivity is defined by an exclusion rule rather than by a positive criterion: cells responding to more than five image sets are dropped so that promiscuous units cannot dominate the counts Quotation withheld because this record is not cleared for redistribution. responsiveness requires three conditions together — a five-SD threshold, a minimum absolute spike count, and a significance test — so no single loose criterion carries a unit through Quotation withheld because this record is not cleared for redistribution. the recency contrast is built into the stimulus set: experimenters are recent acquaintances and family remote ones, which turns the design into a test bearing on consolidation theory Quotation withheld because this record is not cleared for redistribution. the counterargument to their own consolidation inference is written out by the authors rather than left to a critic Quotation withheld because this record is not cleared for redistribution. duplicate views of the same person or landmark are dropped so that no category can win by being represented more often Quotation withheld because this record is not cleared for redistribution. because image counts differ by patient and category, the metric is the proportion of images that elicited a response rather than the count Quotation withheld because this record is not cleared for redistribution. a trivial face/non-face judgment is imposed purely to guarantee attention, not to measure anything Quotation withheld because this record is not cleared for redistribution. the amygdala result is read against the grain of the paper's own thesis, as novelty and emotional salience rather than relevance Quotation withheld because this record is not cleared for redistribution. single units are separated from multiunits by four spike-train criteria including an explicit refractory-period check Quotation withheld because this record is not cleared for redistribution. Patients were never asked whether the images evoked episodic memories, so the recent-versus-remote memory question cannot be settled by the data. what this limits: the recent-versus-remote memory question: BECAUSE WE DID NOT ASK OUR PATIENTS IF THE IMAGES WE SHOWED THEM GENERATED EPISODIC MEMORIES, WE CANNOT ADDRESS THIS ISSUE DIRECTLY WITH OUR CURRENT STUDY Quotation withheld because this record is not cleared for redistribution. Response counts per MTL region were low, so the regional differences must be read cautiously. what this limits: the regional comparisons: response counts per MTL region were low Quotation withheld because this record is not cleared for redistribution. The null result for landmarks is inconclusive because no personally familiar landmarks were included in the stimulus set. what this limits: the landmark null: THOUGH WE DID NOT FIND ANY SIGNIFICANT EFFECTS OF FAMILIARITY WITH RESPECT TO LANDMARKS, WE DID NOT INCLUDE PERSONALLY FAMILIAR LANDMARKS SUCH AS THE PATIENT'S HOME, SCHOOL, OR WORK Quotation withheld because this record is not cleared for redistribution. the mechanism the whole account rests on — incidental recollection — was never measured what this limits: the same scope as limitations[0] - incidental recollection, the mechanism the account rests on, was never measured because patients were not asked Quotation withheld because this record is not cleared for redistribution. the faces-versus-landmarks asymmetry may be an artefact of the stimulus set, because no personally familiar landmarks were included duplicate of: limitations[2] · what this limits: the same scope as limitations[2] - the faces-versus-landmarks asymmetry may be a property of the stimulus set rather than of the regions Quotation withheld because this record is not cleared for redistribution. the regional comparisons rest on small response counts and the authors say they must be read with caution what this limits: the regional comparisons: THE NUMBER OF SIGNIFICANT RESPONSES IN EACH AREA WAS RELATIVELY LOW, AND THEREFORE THESE REGIONAL DIFFERENCES MUST BE INTERPRETED WITH CAUTION Quotation withheld because this record is not cleared for redistribution. images of the patients themselves produced almost nothing, so the self category had to be merged into family what this limits: every result reported for the family category, which silently contains the self: Quotation withheld. THEREFORE, WE DID NOT DIFFERENTIATE BETWEEN PICTURES OF THE SELF AND PICTURES OF FAMILY MEMBERS Quotation withheld because this record is not cleared for redistribution. whether the famous-face responses in hippocampus involve personal recollection is left for future work what this limits: the recollection interpretation of the hippocampal responses: FUTURE STUDIES SHOULD ADDRESS THE EXTENT TO WHICH THE SPECIFIC PHOTOGRAPHS ... WERE ACCOMPANIED BY INCIDENTAL RECOLLECTION OF PERSONAL MEMORIES Quotation withheld because this record is not cleared for redistribution. electrode placement was set by clinical criteria what this limits: which structures could be observed: PATIENTS WERE STEREOTACTICALLY IMPLANTED WITH 6-14 DEPTH ELECTRODES ... AIMING AT TARGETS SELECTED USING CLINICAL CRITERIA Quotation withheld because this record is not cleared for redistribution. the self-reference effect, imported as the motivating prediction that personally relevant stimuli should recruit more neurons Quotation withheld because this record is not cleared for redistribution. the sparse-coding expectation, carried across from animal MTL recordings and used to frame what a human selective response means Quotation withheld because this record is not cleared for redistribution. famous faces and names as a probe of semantic memory integrity, reused here as a graded familiarity stimulus set Quotation withheld because this record is not cleared for redistribution. anatomical electrode locations verified by post-placement MRI and by fusing implantation CT with high-resolution imaging eliminates: attributing a response to the wrong medial temporal structure - the verification is imaging taken after the electrodes are in, not the plan they were placed from · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. the order of the pictures and their repetition randomised eliminates: order and repetition effects - a fixed sequence would confound picture identity with when it appeared and how often · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. personal relevance — as connection to the self versus as accumulated shared experience; the paper opens on the first and its result rests on the second Quotation withheld because this record is not cleared for redistribution. familiarity — as long-standing acquaintance (family) versus as recent daily contact (experimenters); the design treats both as personal relevance and finds them equal Quotation withheld because this record is not cleared for redistribution. familiarity versus recollection — in the models discussed, MTL cortex can support the first alone while the hippocampus is required for the second Quotation withheld because this record is not cleared for redistribution. selective — as the cell's own tuning versus as an analysis threshold; here it is the latter, five image sets Quotation withheld because this record is not cleared for redistribution. MTL selectivity — as coding a person versus as coding the associations that person carries; the paper argues for the second Quotation withheld because this record is not cleared for redistribution. amygdala responsiveness — as personal relevance versus as novelty and emotional salience, which order the same stimuli differently Quotation withheld because this record is not cleared for redistribution. claim_type: existence a second reading reaching the same value. Recorded: existence — note: a second reading reaching the same value from a different sentence. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. method: single- and multi-unit recording from depth microwires in four MTL regions while patients viewed images graded by personal relevance, with responsiveness defined by a three-part criterion a second reading DIFFERING from the recorded value. Recorded: electrophysiology — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. phenomenon: sparse selective coding of familiar people by human medial temporal lobe neurons a second reading DIFFERING from the recorded value. Recorded: personal relevance in human medial temporal lobe single-neuron responses — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. builds-on → Quian Quiroga, Reddy, Kreiman, Koch and Fried (2005), Nature 435(7045):1102-1107, on selective invariant MTL responses to famous people Quotation withheld because this record is not cleared for redistribution. extends → multiple trace theory (MTT) of medial temporal lobe memory function Quotation withheld because this record is not cleared for redistribution. extends → Quian Quiroga et al. 2005, that individual MTL neurons respond selectively and invariantly to famous people Quotation withheld because this record is not cleared for redistribution. builds-on → the self-reference effect literature on encoding enhancement Quotation withheld because this record is not cleared for redistribution. supports → multiple trace theory over the standard consolidation model, on the reading that recent and remote acquaintances alike drive hippocampal cells Quotation withheld because this record is not cleared for redistribution. supports → models in which MTL cortex supports familiarity while the hippocampus supports recollection Quotation withheld because this record is not cleared for redistribution. builds-on → evidence that hippocampal cells code relative familiarity after a single presentation Quotation withheld because this record is not cleared for redistribution. critiques → the state of the MTL regional division of labour, as unresolved despite extensive study Quotation withheld because this record is not cleared for redistribution. personal relevance —causes→ selective responsiveness personal relevance selective responsiveness strength of the relation: 0.8 Quotation withheld because this record is not cleared for redistribution. familiarity —distinct-from→ recollection familiarity recollection differs in: THE AXIS IS WHICH STRUCTURE IS NECESSARY FOR WHICH KIND OF RETRIEVAL. 'Several current theoretical models suggest that MTL CORTEX ALONE CAN SUPPORT FAMILIARITY-BASED MEMORY, WHEREAS THE HIPPOCAMPUS IS NECESSARY FOR THE RETRIEVAL OF EPISODIC INFORMATION, OR RECOLLECTION.' The two processes are not distinguished behaviourally here but by a NECESSITY claim about different tissue - so a lesion that spares MTL cortex is the test, and a task that does not separate the two processes cannot run it. · strength of the relation: 0.95 Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but 'Several current theoretical models suggest' the split; attributed. Quotation withheld because this record is not cleared for redistribution. multiple trace theory —contrasted-with→ standard model of consolidation multiple trace theory standard model of consolidation differs in: THE AXIS IS WHETHER HIPPOCAMPAL INVOLVEMENT DEPENDS ON THE AGE OF THE MEMORY. 'Whereas the standard model of consolidation (MCT) PREDICTS that over long periods of time, memories eventually become independent of the hippocampus, the idea that this structure is involved in episodic memory retrieval without regard to the age of the memory [is the alternative].' Both models agree the hippocampus retrieves episodic memories; they differ on whether that stops. A bare 'contrasted-with' loses the variable - memory age - that any experiment would have to manipulate to tell them apart. · strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. hippocampus —part-of→ medial temporal lobe hippocampus medial temporal lobe strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. EVIDENCE CORRECTED (RE-GROUNDED) · experimenters —contrasted-with→ famous faces experimenters famous faces EVIDENCE CORRECTED: RE-GROUNDED. The old span was about familiarity in general. This sentence names both and carries the contrast WITH ITS STATISTICS AND ITS DIRECTION - family members and experimenters 'DID NOT DIFFER (P > 0.5), though together they were more…'. It states a non-difference and a difference in one sentence, and the edge records the second. — strength of the relation: 1 Audit 2026-09-28: DOUBTFUL - read against its span and kept, but familiar individuals versus famous faces; contrasted-with is loose. Quotation withheld because this record is not cleared for redistribution. single units —distinct-from→ multiunits single units multiunits strength of the relation: 1 Quotation withheld because this record is not cleared for redistribution. landmarks —contrasted-with→ famous faces landmarks famous faces differs in: THE AXIS IS WHETHER FAME MODULATES THE RESPONSE, AND ONE SIDE IS A NULL. 'In contrast to cellular responses to faces, WHICH SHOWED A significant preference for famous faces, as compared with unknown faces, there was no difference in the proportion of cells responding to famous versus unknown landmarks (P = 0.27).' Both categories are represented; only one is sensitive to familiarity, and the evidence for the difference is a significant test on one side and a null on the other. · strength of the relation: 0.95 Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span contrasts cell responses to famous landmarks and famous faces; contrasted-with is loose. Quotation withheld because this record is not cleared for redistribution. chi-squared test chi-squared test Quotation withheld because this record is not cleared for redistribution. t-test t-test Quotation withheld because this record is not cleared for redistribution. median median Quotation withheld because this record is not cleared for redistribution. standard deviation standard deviation Quotation withheld because this record is not cleared for redistribution. planned comparisons planned comparisons Quotation withheld because this record is not cleared for redistribution. post-hoc tests post-hoc tests Quotation withheld because this record is not cleared for redistribution. p-value p-value Quotation withheld because this record is not cleared for redistribution. χ 2 χ 2 Quotation withheld because this record is not cleared for redistribution. planned comparisons planned comparisons Quotation withheld because this record is not cleared for redistribution. post-hoc tests post-hoc tests Quotation withheld because this record is not cleared for redistribution. t test t test Quotation withheld because this record is not cleared for redistribution. median number of spikes median number of spikes Quotation withheld because this record is not cleared for redistribution. 4(region) × 4(category) χ 2 analysis 4(region) × 4(category) χ 2 analysis Quotation withheld because this record is not cleared for redistribution. Photographs of the experimenters were the most likely to elicit a response (22%), followed by photographs of the patients and their families (17%). Quotation withheld because this record is not cleared for redistribution. Family members and experimenters were statistically indistinguishable from each other but together beat celebrities, and celebrities in turn beat unknown faces, giving a graded ladder of personal relevance. Quotation withheld because this record is not cleared for redistribution. Familiarity produced no such effect for places: famous landmarks (14%) and unknown landmarks (11%) elicited statistically indistinguishable proportions of responses. Quotation withheld because this record is not cleared for redistribution. Selective excitatory responses were not spread evenly over the MTL: entorhinal cortex yielded fewer responses than either the hippocampus or the parahippocampal cortex. Quotation withheld because this record is not cleared for redistribution. The four MTL regions differed significantly from one another in how they distributed responses across the four face categories. Quotation withheld because this record is not cleared for redistribution. The hippocampus was the one region where celebrities behaved like personally known people, responding more to famous than to unknown faces while family, experimenters and celebrities did not differ from each other. Quotation withheld because this record is not cleared for redistribution. In entorhinal cortex no unit at all responded to unknown faces. Quotation withheld because this record is not cleared for redistribution. In the amygdala the ordering reversed at the top end: experimenters elicited responses more often than family members. Quotation withheld because this record is not cleared for redistribution. Only 3 units responded to images of the patients themselves. Quotation withheld because this record is not cleared for redistribution. Overall, personally relevant photographs are more likely to elicit selective MTL responses than photographs of people the patient has never met. Quotation withheld because this record is not cleared for redistribution. response likelihood was ordered by personal relevance: experimenters 22%, family 17%, celebrities 9%, unknown faces 5% Quotation withheld because this record is not cleared for redistribution. family and experimenters were indistinguishable, but together beat celebrities, which in turn beat unknown faces Quotation withheld because this record is not cleared for redistribution. the familiarity effect held for faces but not for landmarks — 14% famous against 11% unknown Quotation withheld because this record is not cleared for redistribution. only 3 units responded to images of the patients themselves, so self and family were merged Quotation withheld because this record is not cleared for redistribution. the four MTL regions differed in their category response patterns Quotation withheld because this record is not cleared for redistribution. the hippocampus was the only region where famous faces beat unknown faces, with family, experimenters and celebrities not differing from each other Quotation withheld because this record is not cleared for redistribution. entorhinal cortex produced no responses at all to unknown faces Quotation withheld because this record is not cleared for redistribution. in parahippocampal cortex family and experimenters together beat famous faces strongly, and famous did not beat unknown Quotation withheld because this record is not cleared for redistribution. in the amygdala experimenters beat family, and neither the celebrity nor the unknown contrast held — the familiarity ordering broke down Quotation withheld because this record is not cleared for redistribution. selective responses were unevenly distributed across MTL, with entorhinal cortex responding less than hippocampus and parahippocampal cortex Quotation withheld because this record is not cleared for redistribution. an amygdala unit responded to one researcher's photograph and to none of 100+ perceptually similar images Quotation withheld because this record is not cleared for redistribution. the selectivity exclusion removed only 7% of responsive units Quotation withheld because this record is not cleared for redistribution. self-reference effect self-reference effect Quotation withheld because this record is not cleared for redistribution. criterion of selective responsiveness criterion of selective responsiveness Quotation withheld because this record is not cleared for redistribution. response to a picture response to a picture Quotation withheld because this record is not cleared for redistribution. responsive unit responsive unit Quotation withheld because this record is not cleared for redistribution. multiple trace theory (MTT) multiple trace theory (MTT) Quotation withheld because this record is not cleared for redistribution. sparse code sparse code Quotation withheld because this record is not cleared for redistribution. The self-reference effect The self-reference effect Quotation withheld because this record is not cleared for redistribution. selective responsiveness selective responsiveness Quotation withheld because this record is not cleared for redistribution. response response Quotation withheld because this record is not cleared for redistribution. baseline baseline Quotation withheld because this record is not cleared for redistribution. multiple trace theory multiple trace theory Quotation withheld because this record is not cleared for redistribution. standard model of consolidation standard model of consolidation Quotation withheld because this record is not cleared for redistribution. categories of images categories of images Quotation withheld because this record is not cleared for redistribution. category of stimuli category of stimuli Quotation withheld because this record is not cleared for redistribution. proportions of images eliciting responses proportions of images eliciting responses Quotation withheld because this record is not cleared for redistribution. MTL region MTL region Quotation withheld because this record is not cleared for redistribution. median number of spikes median number of spikes Quotation withheld because this record is not cleared for redistribution. baseline baseline Quotation withheld because this record is not cleared for redistribution. 2,330 — total units recorded from 16 patients over 34 sessions across four MTL regions Quotation withheld because this record is not cleared for redistribution. 153 units — units meeting the selective-responsiveness criterion and entering the category comparisons Quotation withheld because this record is not cleared for redistribution. 7% — share of the 165 responsive units discarded by the selectivity criterion (12 units responding to more than 5 pictures) Quotation withheld because this record is not cleared for redistribution. 22% — proportion of experimenter photographs that generated a selective response, the highest of any category Quotation withheld because this record is not cleared for redistribution. 9% — proportion of famous-face images generating responses, versus 5% for unknown faces Quotation withheld because this record is not cleared for redistribution. 14% — proportion of famous landmarks generating responses, statistically indistinguishable from the 11% for unknown landmarks Quotation withheld because this record is not cleared for redistribution. χ 2 (9) = 32.3, P < 0.0001 — test statistic for the region-by-category interaction showing regions differ in their response patterns Quotation withheld because this record is not cleared for redistribution. 28 kHz — digital sampling rate of the microwire signals, bandpass filtered between 1 and 9 kHz Quotation withheld because this record is not cleared for redistribution. 2,330 units — total recorded, 874 single and 1,456 multiunits Quotation withheld because this record is not cleared for redistribution. 153 units — selective responsive units after the five-set exclusion, from 165 responsive Quotation withheld because this record is not cleared for redistribution. 22% / 17% / 9% / 5% — response rates for experimenters, family, celebrities, unknown faces Quotation withheld because this record is not cleared for redistribution. 14% vs 11% — famous against unknown landmark response rates, not significantly different Quotation withheld because this record is not cleared for redistribution. 3 units — responses to images of the patients themselves Quotation withheld because this record is not cleared for redistribution. sixteen patients, 34 sessions — the sample Quotation withheld because this record is not cleared for redistribution. 6–14 depth electrodes — electrodes implanted per patient, sited by clinical criteria Quotation withheld because this record is not cleared for redistribution. nine 40-μm microwires — microwires per electrode tip, the ninth serving as reference Quotation withheld because this record is not cleared for redistribution. 28 kHz, 1 to 9 kHz — sampling rate and bandpass filter Quotation withheld because this record is not cleared for redistribution. 5 standard deviations — the responsiveness threshold above baseline Quotation withheld because this record is not cleared for redistribution. 6 times for 1 s — repetitions and duration per image Quotation withheld because this record is not cleared for redistribution. 1.5° — visual angle subtended by each image Quotation withheld because this record is not cleared for redistribution. <1% spikes within less than 3 ms ISI — the refractory-period criterion for classifying a cluster as a single unit Quotation withheld because this record is not cleared for redistribution. 1 and 2 weeks — how long patients remained implanted on the ward Quotation withheld because this record is not cleared for redistribution. 100+ — perceptually similar stimuli the example amygdala unit did not respond to Quotation withheld because this record is not cleared for redistribution.

The full text of this article is not redistributable, so it is not included here. The evidence sentences are withheld with it; the tag layer and its grounding status remain. The article itself is at https://doi.org/10.1073/pnas.0902319106.