Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity

According to dual-process signal detection (DPSD) theories, short and long-term recognition memory draw upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to these processes but frequency-specific neuronal activities are considered to play a ke...

Full description

Bibliographic Details
Main Authors: Wu, Z, Kavanova, M, Hickman, L, Boschin, E, Galeazzi, JM, Verhagen, L, Ainsworth, M, Pedreira, C, Buckley, MJ
Format: Journal article
Language:English
Published: Wiley 2021
_version_ 1826301510220251136
author Wu, Z
Kavanova, M
Hickman, L
Boschin, E
Galeazzi, JM
Verhagen, L
Ainsworth, M
Pedreira, C
Buckley, MJ
author_facet Wu, Z
Kavanova, M
Hickman, L
Boschin, E
Galeazzi, JM
Verhagen, L
Ainsworth, M
Pedreira, C
Buckley, MJ
author_sort Wu, Z
collection OXFORD
description According to dual-process signal detection (DPSD) theories, short and long-term recognition memory draw upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to these processes but frequency-specific neuronal activities are considered to play a key role. In Experiment 1, non-human primate (NHP) local field potential (LFP) electrophysiological recordings in macaque left dorsolateral PFC (dlPFC) revealed performance-related differences in a low beta frequency range during the sample presentation phase of a visual object recognition memory task. Experiment 2 employed a similar task in humans and targeted left dlPFC (and vertex as a control) with repetitive transcranial magnetic stimulation (rTMS) at 12.5Hz during occasional sample presentations. This low beta-frequency rTMS to dlPFC decreased DPSD derived indices of recollection, but not familiarity, in subsequent memory tests of the targeted samples after short delays. The same number of rTMS pulses over the same total duration albeit at a random frequency had no effect on either recollection or familiarity. Neither stimulation protocol had any causal effect upon behaviour when targeted to the control site (vertex). In this study our hypotheses for our human TMS study were derived from our observations in NHPs; this approach might inspire further translational research through investigation of homologous brain regions and tasks across species using similar neuroscientific methodologies to advance the neural mechanism of recognition memory in primates.
first_indexed 2024-03-07T05:33:31Z
format Journal article
id oxford-uuid:e316933b-d598-4115-bd01-e57f0ded9fb1
institution University of Oxford
language English
last_indexed 2024-03-07T05:33:31Z
publishDate 2021
publisher Wiley
record_format dspace
spelling oxford-uuid:e316933b-d598-4115-bd01-e57f0ded9fb12022-03-27T10:06:28ZLow beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarityJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:e316933b-d598-4115-bd01-e57f0ded9fb1EnglishSymplectic ElementsWiley2021Wu, ZKavanova, MHickman, LBoschin, EGaleazzi, JMVerhagen, LAinsworth, MPedreira, CBuckley, MJAccording to dual-process signal detection (DPSD) theories, short and long-term recognition memory draw upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to these processes but frequency-specific neuronal activities are considered to play a key role. In Experiment 1, non-human primate (NHP) local field potential (LFP) electrophysiological recordings in macaque left dorsolateral PFC (dlPFC) revealed performance-related differences in a low beta frequency range during the sample presentation phase of a visual object recognition memory task. Experiment 2 employed a similar task in humans and targeted left dlPFC (and vertex as a control) with repetitive transcranial magnetic stimulation (rTMS) at 12.5Hz during occasional sample presentations. This low beta-frequency rTMS to dlPFC decreased DPSD derived indices of recollection, but not familiarity, in subsequent memory tests of the targeted samples after short delays. The same number of rTMS pulses over the same total duration albeit at a random frequency had no effect on either recollection or familiarity. Neither stimulation protocol had any causal effect upon behaviour when targeted to the control site (vertex). In this study our hypotheses for our human TMS study were derived from our observations in NHPs; this approach might inspire further translational research through investigation of homologous brain regions and tasks across species using similar neuroscientific methodologies to advance the neural mechanism of recognition memory in primates.
spellingShingle Wu, Z
Kavanova, M
Hickman, L
Boschin, E
Galeazzi, JM
Verhagen, L
Ainsworth, M
Pedreira, C
Buckley, MJ
Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity
title Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity
title_full Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity
title_fullStr Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity
title_full_unstemmed Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity
title_short Low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation, at a task related frequency observed in local field potentials in homologous macaque cortex, impairs subsequent recollection but not familiarity
title_sort low beta repetitive transcranial magnetic stimulation to human dorsolateral prefrontal cortex during object recognition memory sample presentation at a task related frequency observed in local field potentials in homologous macaque cortex impairs subsequent recollection but not familiarity
work_keys_str_mv AT wuz lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT kavanovam lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT hickmanl lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT boschine lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT galeazzijm lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT verhagenl lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT ainsworthm lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT pedreirac lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity
AT buckleymj lowbetarepetitivetranscranialmagneticstimulationtohumandorsolateralprefrontalcortexduringobjectrecognitionmemorysamplepresentationatataskrelatedfrequencyobservedinlocalfieldpotentialsinhomologousmacaquecorteximpairssubsequentrecollectionbutnotfamiliarity