Neural Substrates of Forward and Backward Associative Priming: A Functional MRI Study

Sarah Terrien, Fabien Gierski, Stéphanie Caillies, Véronique Baltazart, Christophe Portefaix, Laurent Pierot, Chrystel Besche-Richard

1Université de Reims Champagne-Ardenne, Laboratoire Cognition, Santé, Socialisation C2S EA 6291, Reims, France 2Institut Universitaire de France, Paris, France.
1Université de Reims Champagne-Ardenne, Laboratoire Cognition, Santé, Socialisation C2S EA 6291, Reims, France 2Service de Psychiatrie des Adultes, H?pital Robert Debré, CHU de Reims, Reims, France.
1Université de Reims Champagne-Ardenne, Laboratoire Cognition, Santé, Socialisation C2S EA 6291, Reims, France 2Service de Psychiatrie des Adultes, H?pital Robert Debré, CHU de Reims, Reims, France 3P?le d’Imagerie Médicale, H?pital Maison-Blanche, CHU de Reims, Reims, France.
P?le d’Imagerie Médicale, H?pital Maison-Blanche, CHU de Reims, Reims, France.
Université de Reims Champagne-Ardenne, Laboratoire Cognition, Santé, Socialisation C2S EA 6291, Reims, France.

DOI: 10.4236/psych.2013.410A007                

Abstract

Forward associative priming results of an association moves from the prime to the target whereas backward associative priming results of an association from the target to the prime (Koivisto, 1998). Little is known about this dissociation of process and the associated cerebral substrates. Fourteen healthy participants were included in this study. The task consisted in a lexical decision task using an fMRI-adapted semantic priming paradigm. Contrasts between forward related and forward unrelated conditions showed activation in the left temporal gyrus, left inferior prefrontal cortex, fusiform gyrus and occipital regions and cerebellum. Investigation of the different patterns of activation between forward and backward priming shows significant results: during the contrast between the forward priming effect and the backward priming effect, we observe a deactivation of BOLD response in temporal and frontal areas, which may reflect the post-lexical integration process. So, areas responsible for language and for decoding spelling seem not to be involved in the backward process. An adaptation of this research in event-related brain potentials is underway to better explore the temporality of post-lexical process.

Keywords

Semantic Memory; Forward and Backward Priming; fMRI; Left Superior Temporal Gyrus; Post-Lexical Integration

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Argyropoulos, G. (2011). Cerebellar theta-burst stimulation selectively enhances lexical associative priming. Cerebellum, 10, 540-550. http://dx.doi.org/10.1007/s12311-011-0269-y [Google Scholar] [CrossRef] [PubMed]
[2]	Behrmann, M., Nelson, J. J., & Sekuler, E. B. (1998). Visual complexity in letter-by-letter reading: “Pure” alexia is not pure. Neuropsychologia, 36, 1115-1132. http://dx.doi.org/10.1016/S0028-3932(98)00005-0 [Google Scholar] [CrossRef]
[3]	Bellebaum, C., & Daum, I. (2011). Mechanisms of cerebellar involvement in associative learning. Cortex, 47, 128-136. http://dx.doi.org/10.1016/j.cortex.2009.07.016 [Google Scholar] [CrossRef] [PubMed]
[4]	Besche, C., Passerieux, C., Segui, J., Sarfati, Y., Laurent, J. P., & Hardy-Baylé, M. C. (1997). Syntactic and semantic processing in schizophrenic patients evaluated by lexical-decision tasks. Neuropsychology, 4, 498-505. http://dx.doi.org/10.1037/0894-4105.11.4.498 [Google Scholar] [CrossRef]
[5]	Blumstein, S. E., Milberg, W., & Shrier, R. (1982). Semantic processing in aphasia: Evidence from an auditory lexical decision task. Brain and Language, 17, 301-315. http://dx.doi.org/10.1016/0093-934X(82)90023-2 [Google Scholar] [CrossRef]
[6]	Catani, M., Dell’Acqua, F., Vergani, F., Malik, F., Hodge, H., Roy, P., et al. (2012). Short frontal lobe connections of the human brain. Cortex, 48, 273-291. http://dx.doi.org/10.1016/j.cortex.2011.12.001 [Google Scholar] [CrossRef] [PubMed]
[7]	Chwilla, D. J., Hagoort, P., & Brown, C. M. (1998). The mechanism underlying backward priming in a lexical decision task: Spreading activation versus semantic matching. The Quarterly Journal of Experimental Psychology A: Human Experimental Psychology, 51A, 531-560. http://dx.doi.org/10.1080/027249898391521 [Google Scholar] [CrossRef]
[8]	Copland, D. A., de Zubicaray, G. I., McMahon, K., Wilson, S. J., Eastburn, M., & Chenery, H. J. (2003). Brain activity during automatic semantic priming revealed by event-related functional magnetic resonance imaging. NeuroImage, 20, 302-310. http://dx.doi.org/10.1016/S1053-8119(03)00279-9 [Google Scholar] [CrossRef]
[9]	Daselaar, S., Rombouts, S., Veltman, D., Raaijmakers, J., Lazeron, R., & Jonker, C. (2001). Parahippocampal activation during successful recognition of words: A self-paced event-related fMRI study. Neuro-Image, 13, 1113-1120. http://dx.doi.org/10.1006/nimg.2001.0758 [Google Scholar] [CrossRef] [PubMed]
[10]	Franklin, M. S., Dien, J., Neely, H. N., Huber, E., & Waterson, L. D. (2007). Semantic priming modulates the N400, N300, and N400RP. Clinical Neurophysiology, 118, 1053-1068. http://dx.doi.org/10.1016/j.clinph.2007.01.012 [Google Scholar] [CrossRef] [PubMed]
[11]	Gainotti, G. (2006). Anatomical functional and cognitive determinants of semantic memory disorders. Neuroscience and Biobehavioral Reviews, 30, 577-594. http://dx.doi.org/10.1016/j.neubiorev.2005.11.001 [Google Scholar] [CrossRef] [PubMed]
[12]	Gebhart, A. L., Petersen, S. E., & Thach, W. T. (2002). Role of the posterolateral cerebellum in language. In S. M. Highstein, & W. Thach (Eds.), The cerebellum: Recent developments in cerebellar research (pp. 318-333). New York: New York Academy of Sciences.
[13]	Gordon, N. (1996). Speech, language, and the cerebellum. European Journal of Disorders of Communication, 31, 359-367. http://dx.doi.org/10.3109/13682829609031327 [Google Scholar] [CrossRef] [PubMed]
[14]	Hagoort, P. (1993). Impairments of lexical-semantic processing in aphasia: Evidence from the processing of lexical ambiguities. Brain and Language, 45, 189-232. http://dx.doi.org/10.1006/brln.1993.1043 [Google Scholar] [CrossRef] [PubMed]
[15]	Hagoort, P. (1997). Semantic priming in Broca’s aphasics at a short SOA: No support for an automatic access deficit. Brain and Language, 56, 287-300. http://dx.doi.org/10.1006/brln.1997.1849 [Google Scholar] [CrossRef] [PubMed]
[16]	Henik, A., Dronkers, N. F., & Knight, R. T. (1993). Differential effects of semantic and identity priming in patients with left and right hemisphere lesions. Journal of Cognition and Neuroscience, 5, 45-55. http://dx.doi.org/10.1162/jocn.1993.5.1.45 [Google Scholar] [CrossRef] [PubMed]
[17]	Kahan, T. A., Neely, J. H., & Forsythe, W. J. (1999). Dissociated backward priming effects in lexical decision and pronunciation tasks. Psychonomic Bulletin and Review, 6, 105-110. http://dx.doi.org/10.3758/BF03210816 [Google Scholar] [CrossRef]
[18]	Kandhadai, P., & Federmeier, K. D. (2010). Automatic and controlled aspects of lexical associative processing in the two cerebral hemispheres. Psychophysiology, 47, 774-785. http://dx.doi.org/10.1111/j.1469-8986.2009.00969.x [Google Scholar] [CrossRef] [PubMed]
[19]	Ketteler, D., Kastrau, F., Vohn, R., & Huber, W. (2008). The subcortical role of language processing. High level linguistic features such as ambiguity-resolution and the human brain: An fMRI study. Neuro-Image, 39, 2002-2009. http://dx.doi.org/10.1016/j.neuroimage.2007.10.023 [Google Scholar] [CrossRef] [PubMed]
[20]	Koivisto, M. (1998). Backward priming and postlexical processing in the right hemisphere. Laterality, 3, 21-40. http://dx.doi.org/10.1080/135765098397386 [Google Scholar] [CrossRef]
[21]	Koriat, A. (1981). Semantic facilitation in lexical decision as a function of prime-target association. Memory and Cognition, 9, 587-598. http://dx.doi.org/10.3758/BF03202353 [Google Scholar] [CrossRef]
[22]	Leiner, H. C., Leiner, A. L., & Dow, R. S. (1993). Cognitive and language functions of the human cerebellum. Trends in Neurosciences, 16, 444-447. http://dx.doi.org/10.1016/0166-2236(93)90072-T [Google Scholar] [CrossRef]
[23]	Maldjian, J. A., Laurienti, P. J., & Burdette, J. H. (2004). Precentralgyrus discrepancy in electronic versions of the Talairach atlas. NeuroImage, 21, 450-455. http://dx.doi.org/10.1016/j.neuroimage.2003.09.032 [Google Scholar] [CrossRef] [PubMed]
[24]	Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlasbased interrogation of fMRI data sets. NeuroImage, 19, 1233-1239. http://dx.doi.org/10.1016/S1053-8119(03)00169-1 [Google Scholar] [CrossRef]
[25]	Marien, P., Engelborghs, S., & De Deyn, P. (2001). Cerebellar neuroncognition: A new avenue. ActaNeurologicaBelgica, 101, 96-109.
[26]	Matsumoto, A., Iidaka, T., Haneda, K., Okada, T., & Sadato, N. (2005). Linking semantic priming effect in functional MRI and event-related potentials. NeuroImage, 24, 624-634. http://dx.doi.org/10.1016/j.neuroimage.2004.09.008 [Google Scholar] [CrossRef] [PubMed]
[27]	Meyer, D. E., & Schvaneveldt, R. W. (1971). Facilitation in recognizing pairs of words: Evidence of a dependence between retrieval operations. Journal of Experimental Psychology, 90, 227-234. http://dx.doi.org/10.1037/h0031564 [Google Scholar] [CrossRef] [PubMed]
[28]	Milberg, W., Blumstein, S. E., Katz, D., Gershberg, F., & Brown, T. (1995). Semantic facilitation in aphasia: Effects of time and expectancy. Journal of Cognition and Neuroscience, 7, 33-50. http://dx.doi.org/10.1162/jocn.1995.7.1.33 [Google Scholar] [CrossRef] [PubMed]
[29]	Mummery, C. J., Shallice, T., & Price, C. J. (1999). Dual-process model in semantic priming: A functional imaging perspective. NeuroImage, 9, 516-525. http://dx.doi.org/10.1093/cercor/bhp055 [Google Scholar] [CrossRef] [PubMed]
[30]	Neely, J. H. (1991). Semantic priming effects in visual word recognition: A selective review of current findings and theories. In D. Besner, & G. W. Humphreys (Eds.), Basic processes in reading: Visual word recognition (pp. 264-336). Hillsdale, NJ: Lawrence Erlbaum Associates, Inc.
[31]	Neely, J. H., Keefe, D. E., & Ross, K. L. (1989). Semantic priming in the lexical decision task: Roles of prospective prime-generated expectancies and retrospective semantic matching. Journal of Experimental Psychology: Learning, Memory, and Cognition, 15, 1003-1019. http://dx.doi.org/10.1037/0278-7393.15.6.1003 [Google Scholar] [CrossRef]
[32]	Nobre, A. C., Allison, T., & McCarthy, G. J. (1994).Word recognition in the human inferior temporal lobe. Nature, 372, 260-273. http://dx.doi.org/10.1038/372260a0 [Google Scholar] [CrossRef] [PubMed]
[33]	Nobre, A. C., & McCarthy, G. J. (1995). Language-related field potentials in the anteriormedial temporal lobe: II. Effects of word type and semantic priming. Journal of Neuroscience, 15, 1090-2008.
[34]	O’Hare, A. J., Dien, J., Waterson, L. D., & Savage, C. R. (2008). Activation of the posterior cingulate by semantic priming: A co-Registered ERP/fMRI study. Brain Research, 1189, 97-114. http://dx.doi.org/10.1016/j.brainres.2007.10.095 [Google Scholar] [CrossRef] [PubMed]
[35]	Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97-114. http://dx.doi.org/10.1016/0028-3932(71)90067-4 [Google Scholar] [CrossRef] [PubMed]
[36]	Philipose, L. E., Gottesman, R. F., Newhart, M., Kleinman, J. T., Herskovits, E. H., Pawlak, M. A., et al. (2007). Neural regions essential for reading and spelling of words and pseudowords. Annals of Neurology, 62, 481-492. http://dx.doi.org/10.1002/ana.21182 [Google Scholar] [CrossRef] [PubMed]
[37]	Pulvermüller, F. (2012). Meaning and the brain: The neurosemantics of referential, interactive, and combinatorial knowledge. Journal of Neurolinguistics, 25, 423-459. http://dx.doi.org/10.1016/j.jneuroling.2011.03.004 [Google Scholar] [CrossRef]
[38]	Rossel, S. L., Bullmore, E. T., Williams, S. C. R., & David, A. S. (2001). Brain activation during automatic and controlled processing of semantic relations: A priming experiment using lexical-decision. Neuropsychologia, 39, 1167-1176. http://dx.doi.org/10.1016/S0028-3932(01)00049-5 [Google Scholar] [CrossRef]
[39]	Sabb, F. W., Bilder, R. M., Chou, M., & Bookheimer, S. Y. (2007). Working memory effects on semantic processing: Priming differences in pars orbitalis. NeuroImage, 37, 311-322. http://dx.doi.org/10.1016/j.neuroimage.2007.04.050 [Google Scholar] [CrossRef] [PubMed]
[40]	Sass, K., Krach, S., Sachs, O., & Kircher, T. (2009). Lion-tiger-stripes: Neural correlates of indirect semantic priming across processing modalities. NeuroImage, 45, 224-236. http://dx.doi.org/10.1016/j.neuroimage.2008.10.014 [Google Scholar] [CrossRef] [PubMed]
[41]	Schmahmann, J. D., & Pandya, D. N. (1997). The cerebrocerebellar system. International Review of Neurobiology, 41, 31-60. http://dx.doi.org/10.1016/S0074-7742(08)60346-3 [Google Scholar] [CrossRef]
[42]	Simon, J. S., Koutstaal, W., Pince, S., Wagner, A. D., & Schacter, D. L. (2003). Neural mechanisms of visual object priming: Evidence for perceptual and semantic distinctions in fusiform cortex. NeuroImage, 19, 613-626. http://dx.doi.org/10.1016/S1053-8119(03)00096-X [Google Scholar] [CrossRef]
[43]	Starrfelt, R., Habekost, T., & Leff, A. (2009). Too little, too late: Reduced visual span and speed characterize pure alexia. Cerebral Cortex, 19, 2880-2890. http://dx.doi.org/10.1093/cercor/bhp059 [Google Scholar] [CrossRef] [PubMed]
[44]	Stowe, L. A., Paans, A. M., Wijers, A. A., Zwarts, F., Mulder, G., & Vaalburg, W. (1999). Sentence comprehension and word repetition: A positron emission tomography investigation. Psychophysiology, 36, 786-801. http://dx.doi.org/10.1111/1469-8986.3660786 [Google Scholar] [CrossRef] [PubMed]
[45]	Timmann, D., Drepper, J., Frings, M., Maschke, M., Richter, S., Gerwig, M., et al. (2010). The human cerebellum contributes to motor, emotional and cognitive associative learning: A review. Cortex, 46, 845-857. http://dx.doi.org/10.1016/j.cortex.2009.06.009 [Google Scholar] [CrossRef] [PubMed]
[46]	Tzourio-Mazoyer, N. N., Landeau, B. B., Papathanassiou, D. D., Crivello, F. F., Etard, O. O., Delcroix, N. N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuro-Image, 15, 273. http://dx.doi.org/10.1006/nimg.2001.0978 [Google Scholar] [CrossRef] [PubMed]
[47]	Wagner, A. D., Paré-Blagoev, E. J., Clark, J., & Poldrack, R. A. (2001). Recovering meaning: Left prefrontal cortex guides controlled semantic retrieval. Neuron, 2, 329-338. http://dx.doi.org/10.1016/S0896-6273(01)00359-2 [Google Scholar] [CrossRef]