[en] Concept typicality is a key semantic dimension supporting the categorical organization of items based on their features, such that typical items share more features with other members of their category than atypical items, which are more distinctive. Typicality effects manifest in better accuracy and faster response times during categorization tasks, but higher performance for atypical items in episodic memory tasks, due to their distinctiveness. At a neural level, typicality has been linked to the anterior temporal lobe (ATL) and the inferior frontal gyrus (IFG) in semantic decision tasks, but patterns of brain activity during episodic memory tasks remain to be understood. We investigated the neural correlates of typicality in semantic and episodic memory to determine the brain regions associated with semantic typicality and uncover effects arising when items are reinstated during retrieval. In an fMRI study, 26 healthy young subjects first performed a category verification task on words representing typical and atypical concepts (encoding), and then completed a recognition memory task (retrieval). In line with previous literature, we observed higher accuracy and faster response times for typical items in the category verification task, while atypical items were better recognized in the episodic memory task. During category verification, univariate analyses revealed a greater involvement of the angular gyrus for typical items and the inferior frontal gyrus for atypical items. During the correct recognition of old items, regions belonging to the core recollection network were activated. We then compared the similarity of the representations from encoding to retrieval (ERS) using Representation Similarity Analyses. Results showed that typical items were reinstated more than atypical ones in several regions including the left precuneus and left anterior temporal lobe (ATL). This suggests that the correct retrieval of typical items requires finer-grained processing, evidenced by greater item-specific reinstatement, which is needed to resolve their confusability with other members of the category due to their higher feature similarity. Our findings confirm the centrality of the ATL in the processing of typicality while extending it to memory retrieval.
Disciplines :
Neurosciences & behavior
Author, co-author :
Delhaye, Emma ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Aging & Memory
Coco, Moreno I; CICPSI, Faculdade de Psicologia, Universidade de Lisboa, Portugal, Department of Psychology, Sapienza, University of Rome, Italy, IRCCS Santa Lucia, Rome, Italy
Bahri, Mohamed Ali ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Aging & Memory ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et revalidation cognitive
Raposo, Ana; CICPSI, Faculdade de Psicologia, Universidade de Lisboa, Portugal
Language :
English
Title :
Typicality in the brain during semantic and episodic memory decisions.
Alves, M., Raposo, A., Is it a bird? Differential effects of concept typicality on semantic memory and episodic recollection. Rev. Port. Psicol. 44 (2015), 65–79, 10.21631/rpp44_65.
Badre, D., Poldrack, R.A., Paré-Blagoev, E.J., Insler, R.Z., Wagner, A.D., Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex. Neuron 47:6 (2005), 907–918, 10.1016/j.neuron.2005.07.023.
Baird, B., Smallwood, J., Gorgolewski, K.J., Margulies, D.S., Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception. J. Neurosci. 33:42 (2013), 16657–16665, 10.1523/JNEUROSCI.0786-13.2013.
Bartlett, Frederic C., Author. (Frederic charles. Remembering : A Study in Experimental and Social Psychology, second ed., 1932, Cambridge University Press., Sir, 1887–1969.
Binder, J.R., Desai, R.H., Graves, W.W., Conant, L.L., Where Is the Semantic System? A Critical Review and Meta-Analysis of 120 Functional Neuroimaging Studies. Cerebral Cortex 19:12 (2009), 2767–2796 https://doi.org/10.1093/cercor/bhp055.
Bird, C.M., Keidel, J.L., Ing, L.P., Horner, A.J., Burgess, N., Consolidation of complex events via reinstatement in posterior cingulate cortex. J. Neurosci. 35:43 (2015), 14426–14434, 10.1523/JNEUROSCI.1774-15.2015.
Bonner, M.F., Peelle, J.E., Cook, P.A., Grossman, M., Heteromodal conceptual processing in the angular gyrus. Neuroimage 71 (2013), 175–186, 10.1016/j.neuroimage.2013.01.006.
Bonner, M.F., Price, A.R., Where is the anterior temporal lobe and what does it do?. J. Neurosci. 33:10 (2013), 4213–4215, 10.1523/JNEUROSCI.0041-13.2013.
Bonnì, S., Veniero, D., Mastropasqua, C., Ponzo, V., Caltagirone, C., Bozzali, M., Koch, G., TMS evidence for a selective role of the precuneus in source memory retrieval. Behav. Brain Res. 282 (2015), 70–75, 10.1016/j.bbr.2014.12.032.
Bonnici, H.M., Richter, F.R., Yazar, Y., Simons, J.S., Multimodal feature integration in the angular gyrus during episodic and semantic retrieval. J. Neurosci. 36:20 (2016), 5462–5471, 10.1523/JNEUROSCI.4310-15.2016.
Borghesani, V., Pedregosa, F., Buiatti, M., Amadon, A., Eger, E., Piazza, M., Word meaning in the ventral visual path : a perceptual to conceptual gradient of semantic coding. Neuroimage 143 (2016), 128–140, 10.1016/j.neuroimage.2016.08.068.
Brett, M., Anton, J.-L., Valabregue, R., Poline, J.-B., Region of Interest Analysis Using an SPM Toolbox. 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan. 2002.
Bruett, H., Calloway, R.C., Tokowicz, N., Coutanche, M.N., Neural pattern similarity across concept exemplars predicts memory after a long delay. Neuroimage, 219, 2020, 10.1016/j.neuroimage.2020.117030 117030.
Bruffaerts, R., De Deyne, S., Meersmans, K., Liuzzi, A.G., Storms, G., Vandenberghe, R., Redefining the resolution of semantic knowledge in the brain : advances made by the introduction of models of semantics in neuroimaging. Neurosci. Biobehav. Rev. 103 (2019), 3–13, 10.1016/j.neubiorev.2019.05.015.
Bruffaerts, R., Dupont, P., Peeters, R., De Deyne, S., Storms, G., Vandenberghe, R., Similarity of fMRI activity patterns in left perirhinal cortex reflects semantic similarity between words. J. Neurosci. 33:47 (2013), 18597–18607, 10.1523/JNEUROSCI.1548-13.2013.
Chen, Y., Shimotake, A., Matsumoto, R., Kunieda, T., Kikuchi, T., Miyamoto, S., Fukuyama, H., Takahashi, R., Ikeda, A., Ralph, Lambon, M, A., The ‘when’ and ‘where’ of semantic coding in the anterior temporal lobe : temporal representational similarity analysis of electrocorticogram data. Cortex 79 (2016), 1–13, 10.1016/j.cortex.2016.02.015.
Clarke, A., Dynamic activity patterns in the anterior temporal lobe represents object semantics. Cognit. Neurosci., 2020, 1–11, 10.1080/17588928.2020.1742678.
Clarke, A., Tyler, L.K., Object-specific semantic coding in human perirhinal cortex. J. Neurosci. 34:14 (2014), 4766–4775, 10.1523/JNEUROSCI.2828-13.2014.
Coutanche, M.N., Thompson-Schill, S.L., Creating concepts from converging features in human cortex. Cerebr. Cortex 25:9 (2015), 2584–2593, 10.1093/cercor/bhu057.
Craik, F.I.M., Lockhart, R.S., Levels of processing : a framework for memory research. J. Verb. Learn. Verb. Behav. 11:6 (1972), 671–684, 10.1016/S0022-5371(72)80001-X.
Davis, T., Poldrack, R.A., Quantifying the internal structure of categories using a neural typicality measure. Cerebr. Cortex 24:7 (2014), 1720–1737, 10.1093/cercor/bht014.
Fairhall, S.L., Caramazza, A., Brain regions that represent amodal conceptual knowledge. J. Neurosci. 33:25 (2013), 10552–10558, 10.1523/JNEUROSCI.0051-13.2013.
Farahibozorg, S.-R., Henson, R.N., Woollams, A.M., Hauk, O., Distinct roles for the anterior temporal lobe and angular gyrus in the spatiotemporal cortical semantic network. Cerebr. Cortex, 2022, bhab501, 10.1093/cercor/bhab501.
Federmeier, K.D., Kutas, M., Schul, R., Age-related and individual differences in the use of prediction during language comprehension. Brain Lang. 115:3 (2010), 149–161, 10.1016/j.bandl.2010.07.006.
Federmeier, K.D., Wlotko, E.W., De Ochoa-Dewald, E., Kutas, M., Multiple effects of sentential constraint on word processing. Brain Res. 1146 (2007), 75–84, 10.1016/j.brainres.2006.06.101.
Folville, A., Bahri, M.A., Delhaye, E., Salmon, E., D'Argembeau, A., Bastin, C., Age-related differences in the neural correlates of vivid remembering. Neuroimage, 206(116336), 2020, 10.1016/j.neuroimage.2019.116336.
Gardini, S., Cornoldi, C., De Beni, R., Venneri, A., Left mediotemporal structures mediate the retrieval of episodic autobiographical mental images. Neuroimage 30:2 (2006), 645–655, 10.1016/j.neuroimage.2005.10.012.
Greenberg, D.L., Verfaellie, M., Interdependence of episodic and semantic memory : evidence from neuropsychology. J. Int. Neuropsychol. Soc. 16:5 (2010), 748–753, 10.1017/S1355617710000676.
Grossman, M., Smith, E.E., Koenig, P., Glosser, G., DeVita, C., Moore, P., McMillan, C., The neural basis for categorization in semantic memory. Neuroimage 17:3 (2002), 1549–1561, 10.1006/nimg.2002.1273.
Herron, J.E., Henson, R.N.A., Rugg, M.D., Probability effects on the neural correlates of retrieval success : an fMRI study. Neuroimage 21:1 (2004), 302–310, 10.1016/j.neuroimage.2003.09.039.
Holmes, S.J., Ellis, A.W., Age of acquisition and typicality effects in three object processing tasks. Vis. Cognit. 13:7–8 (2006), 884–910, 10.1080/13506280544000093.
Höltje, G., Lubahn, B., Mecklinger, A., The congruent, the incongruent, and the unexpected : event-related potentials unveil the processes involved in schematic encoding. Neuropsychologia 131 (2019), 285–293, 10.1016/j.neuropsychologia.2019.05.013.
Hunt, R.R., Precision in memory through distinctive processing. Curr. Dir. Psychol. Sci. 22:1 (2013), 10–15, 10.1177/0963721412463228.
Irish, M., Vatansever, D., Rethinking the episodic-semantic distinction from a gradient perspective. Curr. Opin. Behav. Sci., 7, 2020.
Kiran, S., Ntourou, K., Eubank, M., The effect of typicality on online category verification of inanimate category exemplars in aphasia. Aphasiology 21:9 (2007), 844–866, 10.1080/02687030600743564.
Kriegeskorte, N., Mur, M., Bandettini, P.A., Representational similarity analysis – connecting the branches of systems neuroscience. Front. Syst. Neurosci., 2008, 10.3389/neuro.06.004.2008.
Li, R., Perrachione, T.K., Tourville, J.A., Kiran, S., Representation of semantic typicality in brain activation in healthy adults and individuals with aphasia : a multi-voxel pattern analysis. Neuropsychologia, 158(107893), 2021, 10.1016/j.neuropsychologia.2021.107893.
Liuzzi, A.G., Aglinskas, A., Fairhall, S.L., General and feature-based semantic representations in the semantic network. Sci. Rep., 10(1), 2020, 8931, 10.1038/s41598-020-65906-0.
Liuzzi, A.G., Bruffaerts, R., Dupont, P., Adamczuk, K., Peeters, R., De Deyne, S., Storms, G., Vandenberghe, R., Left perirhinal cortex codes for similarity in meaning between written words : comparison with auditory word input. Neuropsychologia 76 (2015), 4–16, 10.1016/j.neuropsychologia.2015.03.016.
Marques, J.F., The general/specific breakdown of semantic memory and the nature of superordinate knowledge: Insight. Cognit. Neuropsychol., 26, 2007.
Martin, C.B., Douglas, D., Newsome, R.N., Man, L.L.Y., Barense, M., Integrative and distinctive coding of visual and conceptual object features in the ventral visual stream. Elife, 7, 2018.
Oedekoven, C.S.H., Keidel, J.L., Berens, S.C., Bird, C.M., Reinstatement of memory representations for lifelike events over the course of a week. Sci. Rep., 7(1), 2017, 14305, 10.1038/s41598-017-13938-4.
Olman, C.A., Davachi, L., Inati, S., Distortion and signal loss in medial temporal lobe. PLoS One, 4(12), 2009, e8160, 10.1371/journal.pone.0008160.
Oosterhof, N.N., Connolly, A.C., Haxby, J.V., CoSMoMVPA : multi-modal multivariate pattern analysis of neuroimaging data in Matlab/GNU octave. Front. Neuroinf., 10, 2016, 10.3389/fninf.2016.00027.
Patterson, K., Nestor, P.J., Rogers, T.T., Where do you know what you know ? The representation of semantic knowledge in the human brain. Nat. Rev. Neurosci. 8 (2007), 976–988.
Qin, S., van Marle, H.J.F., Hermans, E.J., Fernandez, G., Subjective sense of memory strength and the objective amount of information accurately remembered are related to distinct neural correlates at encoding. J. Neurosci. 31:24 (2011), 8920–8927, 10.1523/JNEUROSCI.2587-10.2011.
Ralph, M.A.L., Jefferies, E., Patterson, K., Rogers, T.T., The neural and computational bases of semantic cognition. Nat. Rev. Neurosci. 18:1 (2017), 42–55, 10.1038/nrn.2016.150.
Raposo, A., Mendes, M., Marques, J.F., The hierarchical organization of semantic memory : executive function in the processing of superordinate concepts. Neuroimage 59:2 (2012), 1870–1878, 10.1016/j.neuroimage.2011.08.072.
Reilly, M., Machado, N., Blumstein, S.E., Distinctive semantic features in the healthy adult brain. Cognit. Affect Behav. Neurosci. 19:2 (2019), 296–308, 10.3758/s13415-018-00668-x.
Renoult, L., Irish, M., Moscovitch, M., Rugg, M.D., From knowing to remembering : the semantic–episodic distinction. Trends Cognit. Sci. 23:12 (2019), 1041–1057, 10.1016/j.tics.2019.09.008.
Richter, F.R., Cooper, R.A., Bays, P.M., Simons, J.S., Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory. Elife, 5, 2016, e18260, 10.7554/eLife.18260.
Rosch, E., Mervis, C.B., Family resemblances : studies in the internal structure of categories. Cognit. Psychol. 7:4 (1975), 573–605, 10.1016/0010-0285(75)90024-9.
Santi, A., Raposo, A., Frade, S., Marques, J.F., Concept typicality responses in the semantic memory network. Neuropsychologia 93 (2016), 167–175, 10.1016/j.neuropsychologia.2016.10.012.
Seghier, M.L., The angular gyrus : multiple functions and multiple subdivisions. Neuroscientist 19:1 (2013), 43–61, 10.1177/1073858412440596.
Souza, C., Garrido, M.V., Horchak, O.V., Carmo, J.C., Conceptual knowledge modulates memory recognition of common items : the selective role of item-typicality. Mem. Cognit., 2021, 10.3758/s13421-021-01213-x.
Sreekumar, V., Nielson, D.M., Smith, T.A., Dennis, S.J., Sederberg, P.B., The experience of vivid autobiographical reminiscence is supported by subjective content representations in the precuneus. Sci. Rep., 8(1), 2018, 14899, 10.1038/s41598-018-32879-0.
St-Laurent, M., Abdi, H., Buchsbaum, B.R., Distributed patterns of reactivation predict vividness of recollection. J. Cognit. Neurosci. 27:10 (2015), 2000–2018, 10.1162/jocn_a_00839.
Tibon, R., Fuhrmann, D., Levy, D.A., Simons, J.S., Henson, R.N., Multimodal integration and vividness in the angular gyrus during episodic encoding and retrieval. J. Neurosci. 39:22 (2019), 4365–4374, 10.1523/JNEUROSCI.2102-18.2018.
Tulving, E., Episodic and semantic memory. Organization of Memory (Tulving&W. Donaldson, 1972, Academic Press, 381–403.
Tulving, E., Memory and consciousness. Can. Psychol. 26:1 (1985), 1–12.
Tulving, E., Rosenbaum, S., What do explanations of the distinctiveness effect need to explain?. R. R. Hunt & J. B. Worthen (Éds.), Distinctiveness and Memory, 2006, Oxford University Press, 406–423, 10.1093/acprof:oso/9780195169669.003.0018.
Visser, M., Jefferies, E., Ralph, Lambon, M, A., Semantic processing in the anterior temporal lobes : a meta-analysis of the functional neuroimaging literature. J. Cognit. Neurosci. 22:6 (2010), 1083–1094, 10.1162/jocn.2009.21309.
von Restorff, H., Uber die wirkung von bereichsbildungen im spurenfeld. Psychol. Forsch. 18 (1933), 299–342.
Wang, T.H., Johnson, J.D., de Chastelaine, M., Donley, B.E., Rugg, M.D., The effects of age on the neural correlates of recollection success, recollection-related cortical reinstatement, and post-retrieval monitoring. Cerebr. Cortex 26:4 (2016), 1698–1714, 10.1093/cercor/bhu333.
Wing, E.A., Ritchey, M., Cabeza, R., Reinstatement of individual past events revealed by the similarity of distributed activation patterns during encoding and retrieval. J. Cognit. Neurosci. 27:4 (2015), 679–691, 10.1162/jocn_a_00740.
Woo, C.W., Krishnan, A., Wager, T.D., Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 91 (2014), 412–419, 10.1016/j.neuroimage.
Woollams, A.M., Apples are not the only fruit : the effects of concept typicality on semantic representation in the anterior temporal lobe. Front. Hum. Neurosci., 6, 2012, 10.3389/fnhum.2012.00085.
Woollams, A.M., Cooper-Pye, E., Hodges, J.R., Patterson, K., Anomia : a doubly typical signature of semantic dementia. Neuropsychologia 46:10 (2008), 2503–2514, 10.1016/j.neuropsychologia.2008.04.005.