Abstract
People tend to close their eyes when trying to retrieve an event or a visual image from memory. However the brain mechanisms behind this phenomenon remain poorly understood. Recently, we showed that during visual mental imagery, auditory areas show a much more robust deactivation than during visual perception. Here we ask whether this is a special case of a more general phenomenon involving retrieval of intrinsic, internally stored information, which would result in crossmodal deactivations in other sensory cortices which are irrelevant to the task at hand. To test this hypothesis, a group of 9 sighted individuals were scanned while performing a memory retrieval task for highly abstract words (i.e., with low imaginability scores). We also scanned a group of 10 congenitally blind, which by definition do not have any visual imagery per se. In sighted subjects, both auditory and visual areas were robustly deactivated during memory retrieval, whereas in the blind the auditory cortex was deactivated while visual areas, shown previously to be relevant for this task, presented a positive BOLD signal. These results suggest that deactivation may be most prominent in task-irrelevant sensory cortices whenever there is a need for retrieval or manipulation of internally stored representations. Thus, there is a task-dependent balance of activation and deactivation that might allow maximization of resources and filtering out of non relevant information to enable allocation of attention to the required task. Furthermore, these results suggest that the balance between positive and negative BOLD might be crucial to our understanding of a large variety of intrinsic and extrinsic tasks including high-level cognitive functions, sensory processing and multisensory integration.
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References
Alain C, McDonald KL (2007) Age-related differences in neuromagnetic brain activity underlying concurrent sound perception. J Neurosci 27:1308–1314
Amedi A, Raz N, Pianka P, Malach R, Zohary E (2003) Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind. Nat Neurosci 6:758–766
Amedi A, Malach R, Pascual-Leone A (2005a) Negative BOLD differentiates visual imagery and perception. Neuron 48:859–872
Amedi A, Merabet LB, Bermpohl F, Pascual-Leone A (2005b) The occipital cortex in the blind. Lessons about plasticity and vision. Curr Dir Psychol Sci 14:306–311
Amedi A, von Kriegstein K, van Atteveldt NM, Beauchamp MS, Naumer MJ (2005c) Functional imaging of human crossmodal identification and object recognition. Exp Brain Res 166:559–571
Amedi A, Stern WM, Camprodon JA, Bermpohl F, Merabet L, Rotman S, Hemond C, Meijer P, Pascual-Leone A (2007) Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex. Nat Neurosci 10:687–689
Baier B, Kleinschmidt A, Muller NG (2006) Cross-modal processing in early visual and auditory cortices depends on expected statistical relationship of multisensory information. J Neurosci 26:12260–12265
Beauchamp MS (2005) See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex. Curr Opin Neurobiol 15:145–153
Bianciardi M, Fukunaga M, van Gelderen P, Horovitz SG, de Zwart JA, Duyn JH (2009) Modulation of spontaneous fMRI activity in human visual cortex by behavioral state. Neuroimage 45:160–168
Boynton GM, Engel SA, Glover GH, Heeger DJ (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci 16:4207–4221
Burton H, Snyder AZ, Diamond JB, Raichle ME (2002) Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. J Neurophysiol 88:3359–3371
Collignon O, Voss P, Lassonde M, Lepore F (2009) Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects. Exp Brain Res 192:343–358
D’Angiulli A, Waraich P (2002) Enhanced tactile encoding and memory recognition in congenital blindness. Int J Rehabil Res 25:143–145
De Volder AG, Bol A, Blin J, Robert A, Arno P, Grandin C, Michel C, Veraart C (1997) Brain energy metabolism in early blind subjects: neural activity in the visual cortex. Brain Res 75:235–244
Driver J, Spence C (1998) Crossmodal attention. Curr Opin Neurobiol 8:245–253
Drzezga A, Grimmer T, Peller M, Wermke M, Siebner H, Rauschecker JP, Schwaiger M, Kurz A (2005) Impaired cross-modal inhibition in Alzheimer disease. PLoS Med 2:e288
Fiez JA (1997) Phonology, semantics, and the role of the left inferior prefrontal cortex. Hum Brain Mapp 5:79–83
Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636–647
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678
Friston KJ, Holmes AP, Worsley KJ (1999) How many subjects constitute a study? Neuroimage 10:1–5
Gabrieli JD, Poldrack RA, Desmond JE (1998) The role of left prefrontal cortex in language and memory. Proc Natl Acad Sci USA 95:906–913
Garg A, Schwartz D, Stevens AA (2007) Orienting auditory spatial attention engages frontal eye fields and medial occipital cortex in congenitally blind humans. Neuropsychologia 45:2307–2321
Golland Y, Bentin S, Gelbard H, Benjamini Y, Heller R, Nir Y, Hasson U, Malach R (2007) Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. Cereb Cortex 17:766–777
Golland Y, Golland P, Bentin S, Malach R (2008) Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems. Neuropsychologia 46:540–553
Gougoux F, Zatorre RJ, Lassonde M, Voss P, Lepore F (2005) A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals. PLoS Biol 3:e27
Greicius MD, Menon V (2004) Default-mode activity during a passive sensory task: uncoupled from deactivation but impacting activation. J Cogn Neurosci 16:1484–1492
Gusnard DA, Raichle ME (2001) Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci 2:685–694
Hairston WD, Hodges DA, Casanova R, Hayasaka S, Kraft R, Maldjian JA, Burdette JH (2008) Closing the mind’s eye: deactivation of visual cortex related to auditory task difficulty. NeuroReport 19:151–154
Hull T, Mason H (1995) Performance of blind-children on digit-span tests. J Vis Impair Blind 89:166–169
Ishai A, Sagi D (1995) Common mechanisms of visual imagery and perception. Science 268:1772–1774
Ishai A, Ungerleider LG, Haxby JV (2000) Distributed neural systems for the generation of visual images. Neuron 28:979–990
Kaas JH, Hackett TA, Tramo MJ (1999) Auditory processing in primate cerebral cortex. Curr Opin Neurobiol 9:164–170
Kawashima R, O’Sullivan BT, Roland PE (1995) Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: closing the “mind’s eye”. Proc Natl Acad Sci US 92:5969–5972
Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A (2003) Spontaneously emerging cortical representations of visual attributes. Nature 425:954–956
Klein I, Dubois J, Mangin JF, Kherif F, Flandin G, Poline JB, Denis M, Kosslyn SM, Le Bihan D (2004) Retinotopic organization of visual mental images as revealed by functional magnetic resonance imaging. Brain Res Cogn Brain Res 22:26–31
Kosslyn SM, Alpert NM, Thompson WL, Maljkovic V, Weise SB, Chabris CF, Hamilton SE, Rauch SL, Buonanno FS (1993) Visual mental imagery activates topographically organized visual cortex: Pet investigations. J Cogn Neurosci 5:263–287
Kosslyn SM, Pascual-Leone A, Felician O, Camposano S, Keenan JP, Thompson WL, Ganis G, Sukel KE, Alpert NM (1999) The role of area 17 in visual imagery: convergent evidence from PET and rTMS. Science 284:167–170
Kreiman G, Koch C, Fried I (2000) Imagery neurons in the human brain. Nature 408:357–361
Lambert S, Sampaio E, Mauss Y, Scheiber C (2004) Blindness and brain plasticity: contribution of mental imagery? An fMRI study. Brain Res Cogn Brain Res 20:1–11
Laurienti PJ (2004) Deactivations, global signal, and the default mode of brain function. J Cogn Neurosci 16:1481–1483
Laurienti PJ, Burdette JH, Wallace MT, Yen YF, Field AS, Stein BE (2002) Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci 14:420–429
Lewis JW, Beauchamp MS, DeYoe EA (2000) A comparison of visual and auditory motion processing in human cerebral cortex. Cereb Cortex 10:873–888
Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769
Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci USA 104:13170–13175
Mazoyer B, Zago L, Mellet E, Bricogne S, Etard O, Houde O, Crivello F, Joliot M, Petit L, Tzourio-Mazoyer N (2001) Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res Bull 54:287–298
Mechelli A, Price CJ, Friston KJ, Ishai A (2004) Where bottom-up meets top-down: neuronal interactions during perception and imagery. Cereb Cortex 14:1256–1265
Mozolic JL, Joyner D, Hugenschmidt CE, Peiffer AM, Kraft RA, Maldjian JA, Laurienti PJ (2008) Cross-modal deactivations during modality-specific selective attention. BMC Neurol 8:35
Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, Gelbard-Sagiv H, Kipervasser S, Andelman F, Neufeld MY, Kramer U, Arieli A, Fried I, Malach R (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11:1100–1108
Noppeney U (2007) The effects of visual deprivation on functional and structural organization of the human brain. Neurosci Biobehav Rev 31:1169–1180
O’Craven KM, Kanwisher N (2000) Mental imagery of faces and places activates corresponding stiimulus-specific brain regions. J Cogn Neurosci 12:1013–1023
Pascual-Leone A, Hamilton R (2001) The metamodal organization of the brain. Prog Brain Res 134:427–445
Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401
Peiffer AM, Hugenschmidt CE, Maldjian JA, Casanova R, Srikanth R, Hayasaka S, Burdette JH, Kraft RA, Laurienti PJ (2009) Aging and the interaction of sensory cortical function and structure. Hum Brain Mapp 30:228–240
Petrides M, Alivisatos B, Meyer E, Evans AC (1993) Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proc Natl Acad Sci USA 90:878–882
Pozar L (1982) Effect of long-term sensory deprivation on recall of verbal material. Stud Psychol 24:311
Pring L (1988) The ‘reverse-generation’ effect: a comparison of memory performance between blind and sighted children. Br J Psychol 79(Pt 3):387–400
Ptito M, Moesgaard SM, Gjedde A, Kupers R (2005) Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. Brain 128:606–614
Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449–476
Raichle ME, Snyder AZ (2007) A default mode of brain function: a brief history of an evolving idea. Neuroimage 37:1083–1090; discussion 1097–1089
Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682
Raz N, Amedi A, Zohary E (2005) V1 activation in congenitally blind humans is associated with episodic retrieval. Cereb Cortex 15:1459–1468
Raz N, Striem E, Pundak G, Orlov T, Zohary E (2007) Superior serial memory in the blind: a case of cognitive compensatory adjustment. Curr Biol 17:1129–1133
Röder B, Rösler F, Neville HJ (2000) Event-related potentials during auditory language processing in congenitally blind and sighted people. Neuropsychologia 38:1482–1502
Röder B, Rösler F, Neville HJ (2001) Auditory memory in congenitally blind adults: a behavioral-electrophysiological investigation. Brain Res Cogn Brain Res 11:289–303
Sadato N, Pascual-Leone A, Grafman J, Ibanez V, Deiber MP, Dold G, Hallett M (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380:526–528
Sathian K (2005) Visual cortical activity during tactile perception in the sighted and the visually deprived. Dev Psychobiol 46:279–286
Sathian K, Zangaladze A (2002) Feeling with the mind’s eye: contribution of visual cortex to tactile perception. Behav Brain Res 135:127–132
Shmuel A, Yacoub E, Pfeuffer J, Van de Moortele PF, Adriany G, Hu X, Ugurbil K (2002) Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36:1195–1210
Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9:569–577
Smits B, Mommers MJC (1976) Differences between blind and sighted children on WISC verbal subtests. New Outlook Blind 70:240–246
Spanos NP, Stam HJ (1979) The elicitation of visual hallucinations via brief instructions in a normal sample. J Nerv Ment Dis 167:488–494
Stein BE, Meredith MA (1993) The merging of the senses. The MIT Press, Cambridge, MA
Stevens WD, Hasher L, Chiew KS, Grady CL (2008) A neural mechanism underlying memory failure in older adults. J Neurosci 28:12820–12824
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York
Tillman MH, Bashaw WL (1968) Multivariate analysis of the WISC scales for blind and sighted children. Psychol Rep 23:523–526
Tomasi D, Ernst T, Caparelli EC, Chang L (2006) Common deactivation patterns during working memory and visual attention tasks: an intra-subject fMRI study at 4 Tesla. Hum Brain Mapp 27:694–705
Wade AR (2002) The negative BOLD signal unmasked. Neuron 36:993–995
Wang K, Jiang T, Yu C, Tian L, Li J, Liu Y, Zhou Y, Xu L, Song M, Li K (2008) Spontaneous activity associated with primary visual cortex: a resting-state FMRI study. Cereb Cortex 18:697–704
Weeks R, Horwitz B, Aziz-Sultan A, Tian B, Wessinger CM, Cohen LG, Hallett M, Rauschecker JP (2000) A positron emission tomographic study of auditory localization in the congenitally blind. J Neurosci 20:2664–2672
Wermke M, Sorg C, Wohlschlager AM, Drzezga A (2008) A new integrative model of cerebral activation, deactivation and default mode function in Alzheimer’s disease. Eur J Nucl Med Mol Imaging 35(Suppl 1):S12–S24
Wessinger CM, VanMeter J, Tian B, Van Lare J, Pekar J, Rauschecker JP (2001) Hierarchical organization of the human auditory cortex revealed by functional magnetic resonance imaging. J Cogn Neurosci 13:1–7
Zangaladze A, Epstein CM, Grafton ST, Sathian K (1999) Involvement of visual cortex in tactile discrimination of orientation. Nature 401:587–590
Zhang M, Weisser VD, Stilla R, Prather SC, Sathian K (2004) Multisensory cortical processing of object shape and its relation to mental imagery. Cogn Affect Behav Neurosci 4:251–259
Acknowledgments
This work was supported by the Human Frontiers Science Program Career Development Award (to AA), an EU-FP7 MC International Reintegration Grant, National Institute for Psychobiology Grant (036/4572) and a GIF-Young Grant (to AA) and by the generous support of the Moscona and the Eliyaho Pen foundations. We wish to thank Z. Tal for very useful discussions and feedback.
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This article is published as part of the Special Issue on Multisensory Integration.
H. Azulay and E. Striem contributed equally to this work.
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Azulay, H., Striem, E. & Amedi, A. Negative BOLD in Sensory Cortices During Verbal Memory: A Component in Generating Internal Representations?. Brain Topogr 21, 221–231 (2009). https://doi.org/10.1007/s10548-009-0089-2
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DOI: https://doi.org/10.1007/s10548-009-0089-2