[en] The prevailing view in human cognitive neuroscience associates the medial temporal lobes (MTLs) with declarative memory. Compelling experimental evidence has, however, demonstrated that these regions are specialized according to the representations processed, irrespective of the cognitive domain assessed. This account was supported by the study of patients with bilateral medial temporal amnesia, who exhibit impairments in perceptual tasks involving complex visual stimuli. Yet, little is known regarding the impact of unilateral MTL damage on complex visual abilities. To address this issue, we administered a visual matching task to 20 patients who underwent left (N = 12) or right (N = 8) anterior temporal lobectomy for drug-resistant epilepsy and to 38 healthy controls. Presentation viewpoint was manipulated to increase feature ambiguity, as this is critical to reveal impairments in perceptual tasks. Similar to control participants, patients with left-sided damage succeeded in all task conditions. In contrast, patients with right-sided damage had decreased accuracy compared with that of the other two groups, as well as increased response time. Notably, the accuracy of those with right-sided damage did not exceed chance level when feature ambiguity was high (i.e., when stimuli were presented from different viewpoints) for the most complex classes of stimuli (i.e., scenes and buildings, compared with single objects). The pattern reported in bilateral patients in previous studies was therefore reproduced in patients with right, but not left, resection. These results suggest that the complex visual-representation functions supported by the MTL are right-lateralized, and raise the question as to how the representational account of these regions applies to representations supported by left MTL regions.
Disciplines :
Neurosciences & behavior
Author, co-author :
Gardette, Jeremy ; LPNC, CNRS, UMR 5105, Université Grenoble Alpes, Université Savoie Mont Blanc, Grenoble, France
Hot, Pascal; LPNC, CNRS, UMR 5105, Université Grenoble Alpes, Université Savoie Mont Blanc, Grenoble, France ; Institut Universitaire de France, Paris, France
Language :
English
Title :
Complex visual discrimination is impaired after right, but not left, anterior temporal lobectomy.
The authors thank the Grenoble-Alpes and Saint-Étienne Nord University Hospitals for providing material support and allowing access to the patients. We also thank the Savoie-Mont Blanc University for financial support, and the MSH-Alpes SCREEN platform for help in recruiting volunteers for the control group.The authors thank the Grenoble‐Alpes and Saint‐Étienne Nord University Hospitals for providing material support and allowing access to the patients. We also thank the Savoie‐Mont Blanc University for financial support, and the MSH‐Alpes SCREEN platform for help in recruiting volunteers for the control group.
Allen, R. J. (2018). Classic and recent advances in understanding amnesia. F1000Research, 7, 331. https://doi.org/10.12688/f1000research.13737.1
Aly, M., Ranganath, C., & Yonelinas, A. P. (2013). Detecting changes in scenes: The hippocampus is critical for strength-based perception. Neuron, 78(6), 1127–1137. https://doi.org/10.1016/j.neuron.2013.04.018
Aly, M., & Yonelinas, A. P. (2012). Bridging consciousness and cognition in memory and perception: Evidence for both state and strength processes. PLoS One, 7(1), e30231. https://doi.org/10.1371/journal.pone.0030231
Barense, M. D., Bussey, T. J., Lee, A. C. H., Bussey, T. J., Davies, R. R., Saksida, L. M., Murray, E. A., & Graham, K. S. (2005). Functional specialization in the human medial temporal lobe. Journal of Neuroscience, 25(44), 10239–10246. https://doi.org/10.1523/JNEUROSCI.2704-05.2005
Barense, M. D., Gaffan, D., & Graham, K. S. (2007). The human medial temporal lobe processes online representations of complex objects. Neuropsychologia, 45(13), 2963–2974. https://doi.org/10.1016/j.neuropsychologia.2007.05.023
Barense, M. D., Groen, I. I. A., Lee, A. C. H., Yeung, L.-K., Brady, S. M., Gregori, M., Kapur, N., Bussey, T. J., Saksida, L. M., & Henson, R. N. A. (2012). Intact memory for irrelevant information impairs perception in amnesia. Neuron, 75(1), 157–167. https://doi.org/10.1016/j.neuron.2012.05.014
Barense, M. D., Henson, R. N. A., & Graham, K. S. (2011). Perception and conception: Temporal lobe activity during complex discriminations of familiar and novel faces and objects. Journal of Cognitive Neuroscience, 23(10), 3052–3067. https://doi.org/10.1162/jocn_a_00010
Barense, M. D., Henson, R. N. A., Lee, A. C. H., & Graham, K. S. (2010). Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of viewpoint. Hippocampus, 20(3), 389–401. https://doi.org/10.1002/hipo.20641
Bastin, C., Besson, G., Simon, J., Delhaye, E., Geurten, M., Willems, S., & Salmon, E. (2019). An integrative memory model of recollection and familiarity to understand memory deficits. Behavioral and Brain Sciences, 42, e281. https://doi.org/10.1017/S0140525X19000621
Baxendale, S. A. (1997). The role of the hippocampus in recognition memory. Neuropsychologia, 35(5), 591–598. https://doi.org/10.1016/S0028-3932(96)00123-6
Baxendale, S. A., Thompson, P. J., & Paesschen, W. V. (1998). A test of spatial memory and its clinical utility in the pre-surgical investigation of temporal lobe epilepsy patients. Neuropsychologia, 36(7), 591–602. https://doi.org/10.1016/S0028-3932(97)00163-2
Besson, G., Simon, J., Salmon, E., & Bastin, C. (2020). Familiarity for entities as a sensitive marker of antero-lateral entorhinal atrophy in amnestic mild cognitive impairment. Cortex, 128, 61–72. https://doi.org/10.1016/j.cortex.2020.02.022
Boling, W. W. (2018). Surgical considerations of intractable mesial temporal lobe epilepsy. Brain Sciences, 8(2), 35. https://doi.org/10.3390/brainsci8020035
Brissart, H., Planton, M., Bilger, M., Bulteau, C., Forthoffer, N., Guinet, V., Hennion, S., Kleitz, C., Laguitton, V., Mirabel, H., Mosca, C., Pécheux, N., Pradier, S., Samson, S., Tramoni, E., Voltzenlogel, V., Denos, M., & Boutin, M. (2019). French neuropsychological procedure consensus in epilepsy surgery. Epilepsy & Behavior, 100, 106522. https://doi.org/10.1016/j.yebeh.2019.106522
Buckley, M. J., Booth, M. C. A., Rolls, E. T., & Gaffan, D. (2001). Selective perceptual impairments after perirhinal cortex ablation. Journal of Neuroscience, 21(24), 9824–9836. https://doi.org/10.1523/JNEUROSCI.21-24-09824.2001
Burgess, N., Maguire, E. A., Spiers, H. J., & O’Keefe, J. (2001). A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuro Image, 14(2), 439–453. https://doi.org/10.1006/nimg.2001.0806
Bussey, T. J., & Saksida, L. M. (2002). The organization of visual object representations: A connectionist model of effects of lesions in perirhinal cortex. European Journal of Neuroscience, 15(2), 355–364. https://doi.org/10.1046/j.0953-816x.2001.01850.x
Bussey, T. J., & Saksida, L. M. (2007). Memory, perception, and the ventral visual-perirhinal-hippocampal stream: Thinking outside of the boxes. Hippocampus, 17(9), 898–908. https://doi.org/10.1002/hipo.20320
Bussey, T. J., Saksida, L. M., & Murray, E. A. (2002). Perirhinal cortex resolves feature ambiguity in complex visual discriminations. European Journal of Neuroscience, 15(2), 365–374. https://doi.org/10.1046/j.0953-816x.2001.01851.x
Bussey, T. J., Saksida, L. M., & Murray, E. A. (2005). The perceptual-mnemonic/feature conjunction model of perirhinal cortex function. The Quarterly Journal of Experimental Psychology Section B, 58(3–4), 269–282. https://doi.org/10.1080/02724990544000004
Clarke, A., & Tyler, L. K. (2014). Object-specific semantic coding in human perirhinal cortex. Journal of Neuroscience, 34(14), 4766–4775. https://doi.org/10.1523/JNEUROSCI.2828-13.2014
Devlin, J. T., & Price, C. J. (2007). Perirhinal contributions to human visual perception. Current Biology, 17(17), 1484–1488. https://doi.org/10.1016/j.cub.2007.07.066
Ekstrom, A. D., & Yonelinas, A. P. (2020). Precision, binding, and the hippocampus: Precisely what are we talking about? Neuropsychologia, 138, 107341. https://doi.org/10.1016/j.neuropsychologia.2020.107341
Erez, J., Cusack, R., Kendall, W., & Barense, M. D. (2016). Conjunctive coding of complex object features. Cerebral Cortex, 26(5), 2271–2282. https://doi.org/10.1093/cercor/bhv081
Frisk, V., & Milner, B. (1990). The role of the left hippocampal region in the acquisition and retention of story content. Neuropsychologia, 28(4), 349–359. https://doi.org/10.1016/0028-3932(90)90061-R
Golby, A. J., Poldrack, R. A., Brewer, J. B., Spencer, D., Desmond, J. E., Aron, A. P., & Gabrieli, J. D. E. (2001). Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain, 124(9), 1841–1854. https://doi.org/10.1093/brain/124.9.1841
Hassabis, D., Kumaran, D., & Maguire, E. A. (2007a). Using imagination to understand the neural basis of episodic memory. Journal of Neuroscience, 27(52), 14365–14374. https://doi.org/10.1523/JNEUROSCI.4549-07.2007
Hassabis, D., Kumaran, D., Vann, S. D., & Maguire, E. A. (2007b). Patients with hippocampal amnesia cannot imagine new experiences. Proceedings of the National Academy of Sciences of the United States of America, 104(5), 1726–1731. https://doi.org/10.1073/pnas.0610561104
Hodgetts, C. J., Shine, J. P., Lawrence, A. D., Downing, P. E., & Graham, K. S. (2016). Evidencing a place for the hippocampus within the core scene processing network. Human Brain Mapping, 37(11), 3779–3794. https://doi.org/10.1002/hbm.23275
Hodgetts, C. J., Voets, N. L., Thomas, A. G., Clare, S., Lawrence, A. D., & Graham, K. S. (2017). Ultra-high-field fMRI reveals a role for the subiculum in scene perceptual discrimination. Journal of Neuroscience, 37(12), 3150–3159. https://doi.org/10.1523/JNEUROSCI.3225-16.2017
Igloi, K., Doeller, C. F., Berthoz, A., Rondi-Reig, L., & Burgess, N. (2010). Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proceedings of the National Academy of Sciences of the United States of America, 107(32), 14466–14471. https://doi.org/10.1073/pnas.1004243107
Jones-Gotman, M. (1986). Memory for designs: The hippocampal contribution. Neuropsychologia, 24(2), 193–203. https://doi.org/10.1016/0028-3932(86)90052-7
Kalafat, M., Hugonot-Diener, L., & Poitrenaud, J. (2003). The Mini Mental State (MMS): French standardization and normative data [Standardisation et étalonnage français du « Mini Mental State » (MMS) version GRÉCO]. Revue de Neuropsychologie, 13, 209–236.
Kumaran, D., & Maguire, E. A. (2007). Match mismatch processes underlie human hippocampal responses to associative novelty. Journal of Neuroscience, 27(32), 8517–8524. https://doi.org/10.1523/JNEUROSCI.1677-07.2007
Lawrence, A. V., Cardoza, J., & Ryan, L. (2020). Medial temporal lobe regions mediate complex visual discriminations for both objects and scenes: A process-based view. Hippocampus, 30(8), 879–891. https://doi.org/10.1002/hipo.23203
Lee, A. C. H., Bandelow, S., Schwarzbauer, C., Henson, R. N. A., & Graham, K. S. (2006a). Perirhinal cortex activity during visual object discrimination: An event-related fMRI study. NeuroImage, 33(1), 362–373. https://doi.org/10.1016/j.neuroimage.2006.06.021
Lee, A. C. H., Buckley, M. J., Gaffan, D., Emery, T., Hodges, J. R., & Graham, K. S. (2006b). Differentiating the roles of the hippocampus and perirhinal cortex in processes beyond long-term declarative memory: A double dissociation in dementia. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26(19), 5198–5203. https://doi.org/10.1523/JNEUROSCI.3157-05.2006
Lee, A. C. H., Buckley, M. J., Pegman, S. J., Spiers, H., Scahill, V. L., Gaffan, D., Bussey, T. J., Davies, R. R., Kapur, N., Hodges, J. R., & Graham, K. S. (2005a). Specialization in the medial temporal lobe for processing of objects and scenes. Hippocampus, 15(6), 782–797. https://doi.org/10.1002/hipo.20101
Lee, A. C. H., Bussey, T. J., Murray, E. A., Saksida, L. M., Epstein, R. A., Kapur, N., Hodges, J. R., & Graham, K. S. (2005b). Perceptual deficits in amnesia: Challenging the medial temporal lobe ‘mnemonic’ view. Neuropsychologia, 43(1), 1–11. https://doi.org/10.1016/j.neuropsychologia.2004.07.017
Lee, A. C. H., & Rudebeck, S. R. (2009). Investigating the interaction between spatial perception and working memory in the human medial temporal lobe. Journal of Cognitive Neuroscience, 22(12), 2823–2835. https://doi.org/10.1162/jocn.2009.21396
Lee, A. C. H., Scahill, V. L., & Graham, K. S. (2008). Activating the medial temporal lobe during oddity judgment for faces and scenes. Cerebral Cortex, 18(3), 683–696. https://doi.org/10.1093/cercor/bhm104
Lee, A. C. H., Yeung, L.-K., & Barense, M. D. (2012). The hippocampus and visual perception. Frontiers in Human Neuroscience, 6, 91. https://doi.org/10.3389/fnhum.2012.00091
Lee, C.-H., Ryu, J., Lee, S.-H., Kim, H., & Lee, I. (2016). Functional cross-hemispheric shift between object-place paired associate memory and spatial memory in the human hippocampus. Hippocampus, 26(8), 1061–1077. https://doi.org/10.1002/hipo.22587
Lee, T. M. C., Yip, J. T. H., & Jones-Gotman, M. (2002). Memory deficits after resection from left or right anterior temporal lobe in humans: A meta-analytic review. Epilepsia, 43(3), 283–291. https://doi.org/10.1046/j.1528-1157.2002.09901.x
Lehn, H., Steffenach, H.-A., van Strien, N. M., Veltman, D. J., Witter, M. P., & Håberg, A. K. (2009). A specific role of the human hippocampus in recall of temporal sequences. Journal of Neuroscience, 29(11), 3475–3484. https://doi.org/10.1523/JNEUROSCI.5370-08.2009
Maguire, E. A. (1994). Real-world spatial memory following temporal-lobe surgery in humans. University College Dublin.
Maguire, E. A., Burgess, N., Donnett, J. G., Frackowiak, R. S. J., Frith, C. D., & O'Keefe, J. (1998). Knowing where and getting there: A human navigation network. Science, 280(5365), 921–924. https://doi.org/10.1126/science.280.5365.921
Maguire, E. A., Burke, T., Phillips, J., & Staunton, H. (1996). Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia, 34(10), 993–1001. https://doi.org/10.1016/0028-3932(96)00022-X
Maguire, E. A., Frackowiak, R. S. J., & Frith, C. D. (1997). Recalling routes around London: Activation of the right hippocampus in taxi drivers. Journal of Neuroscience, 17(18), 7103–7110. https://doi.org/10.1523/JNEUROSCI.17-18-07103.1997
Maguire, E. A., & Mummery, C. J. (1999). Differential modulation of a common memory retrieval network revealed by positron emission tomography. Hippocampus, 9(1), 54–61. https://doi.org/10.1002/(SICI)1098-1063(1999)9:1⟨54::AID-HIPO6⟩3.0.CO;2-O
Manjon, J. V., Romero, J. E., Vivo-Hernando, R., Rubio, G., Aparici, F., de la Iglesia-Vaya, M., & Coupe, P. (2022). vol2Brain: A new online pipeline for whole brain MRI analysis (arXiv: 2202.03920), https://doi.org/10.48550/arXiv.2202.03920
Martin, C. B., Douglas, D., Newsome, R. N., Man, L. L., & Barense, M. D. (2018). Integrative and distinctive coding of visual and conceptual object features in the ventral visual stream. eLife, 7, e31873. https://doi.org/10.7554/eLife.31873
Mathôt, S., Schreij, D., & Theeuwes, J. (2012). OpenSesame: An open-source, graphical experiment builder for the social sciences. Behavior Research Methods, 44(2), 314–324. https://doi.org/10.3758/s13428-011-0168-7
McCormick, C., Rosenthal, C. R., Miller, T. D., & Maguire, E. A. (2017). Deciding what is possible and impossible following hippocampal damage in humans. Hippocampus, 27(3), 303–314. https://doi.org/10.1002/hipo.22694
Milner, B. (1972). Disorders of learning and memory after temporal lobe lesions in Man. Neurosurgery, 19(CN_suppl_1), 421–446. https://doi.org/10.1093/neurosurgery/19.CN_suppl_1.421
Milner, B., Corkin, S., & Teuber, H.-L. (1968). Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia, 6(3), 215–234. https://doi.org/10.1016/0028-3932(68)90021-3
Mitrushina, M., Boone, K. B., Razani, J., & D'Elia, L. F. (2005). Handbook of normative data for neuropsychological assessment. Oxford University Press.
Morris, R. G., Abrahams, S., Baddeley, A. D., & Polkey, C. E. (1995). Doors and people: Visual and verbal memory after unilateral temporal lobectomy. Neuropsychology, 9(4), 464–469. https://doi.org/10.1037/0894-4105.9.4.464
Mullally, S. L., Hassabis, D., & Maguire, E. A. (2012). Scene construction in amnesia: An FMRI study. The Journal of Neuroscience, 32(16), 5646–5653. https://doi.org/10.1523/JNEUROSCI.5522-11.2012
Murray, E. A., & Bussey, T. J. (1999). Perceptual–mnemonic functions of the perirhinal cortex. Trends in Cognitive Sciences, 3(4), 142–151. https://doi.org/10.1016/S1364-6613(99)01303-0
Pigott, S., & Milner, B. (1993). Memory for different aspects of complex visual scenes after unilateral temporal- or frontal-lobe resection. Neuropsychologia, 31(1), 1–15. https://doi.org/10.1016/0028-3932(93)90076-C
Pollmann, S., Zinke, W., Baumgartner, F., Geringswald, F., & Hanke, M. (2014). The right temporo-parietal junction contributes to visual feature binding. NeuroImage, 101, 289–297. https://doi.org/10.1016/j.neuroimage.2014.07.021
Rocchetta, A. I. d., & Milner, B. (1993). Strategic search and retrieval inhibition: The role of the frontal lobes. Neuropsychologia, 31(6), 503–524. https://doi.org/10.1016/0028-3932(93)90049-6
Ross, D. A., Sadil, P., Wilson, D. M., & Cowell, R. A. (2018). Hippocampal engagement during recall depends on memory content. Cerebral Cortex, 28(8), 2685–2698. https://doi.org/10.1093/cercor/bhx147
Saksida, L. M., & Bussey, T. J. (2010). The representational-hierarchical view of amnesia: Translation from animal to human. Neuropsychologia, 48(8), 2370–2384. https://doi.org/10.1016/j.neuropsychologia.2010.02.026
Schendan, H. E., Searl, M. M., Melrose, R. J., & Stern, C. E. (2003). An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37(6), 1013–1025. https://doi.org/10.1016/S0896-6273(03)00123-5
Spiers, H. J., Burgess, N., Maguire, E. A., Baxendale, S. A., Hartley, T., Thompson, P. J., & O'Keefe, J. (2001). Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain, 124(12), 2476–2489. https://doi.org/10.1093/brain/124.12.2476
Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171–177. https://doi.org/10.1016/j.nlm.2004.06.005
Stern, C. E., Corkin, S., Gonzalez, R. G., Guimaraes, A. R., Baker, J. R., Jennings, P. J., Carr, C. A., Sugiura, R. M., Vedantham, V., & Rosen, B. R. (1996). The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. Proceedings of the National Academy of Sciences, 93(16), 8660–8665. https://doi.org/10.1073/pnas.93.16.8660
Taylor, K. J., Henson, R. N. A., & Graham, K. S. (2007). Recognition memory for faces and scenes in amnesia: Dissociable roles of medial temporal lobe structures. Neuropsychologia, 45(11), 2428–2438. https://doi.org/10.1016/j.neuropsychologia.2007.04.004
Wechsler, D. (2008). Wechsler adult intelligence scale–fourth edition (WAIS–IV) (Vol. 22(498, p. 1). NCS Pearson.
Wechsler, D. (2009). WMS-IV: Wechsler memory scale. Pearson.
Worsley, C. L., Recce, M., Spiers, H. J., Marley, J., Polkey, C. E., & Morris, R. G. (2001). Path integration following temporal lobectomy in humans. Neuropsychologia, 39(5), 452–464. https://doi.org/10.1016/S0028-3932(00)00140-8
Zeidman, P., & Maguire, E. A. (2016). Anterior hippocampus: The anatomy of perception, imagination and episodic memory. Nature Reviews. Neuroscience, 17(3), 173–182. https://doi.org/10.1038/nrn.2015.24
Zeidman, P., Mullally, S. L., & Maguire, E. A. (2015). Constructing, perceiving, and maintaining scenes: Hippocampal activity and connectivity. Cerebral Cortex, 25(10), 3836–3855. https://doi.org/10.1093/cercor/bhu266